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. 


USDA 
ei 
United States 


Department of 
Agriculture 


Agricultural 
Research 
Service 


August 2000 


110 Years of Biological Control 
Research and Development in the 
United States Department of Agriculture 


1883-1993 


United States 
Department of 
Agriculture 


__ Fy 


WEUCOEVE Cietaiiiie BALy gta 





United States 
Department of 
Agriculture 


Agricultural 
Research 
Service 


August 2000 


110 Years of Biological Control 
Research and Development in the 
United States Department of Agriculture 


1883-1993 


J.R. Coulson, P.V. Vail, M.E. Dix, D.A. Nordlund, and 
W.C. Kauffman, editors 


U.S.D.A., NAL 


AUG 11 2000 
CATALOGING PREP 






Coulson was at the Biological Control Documentation Center, Insect Biocontrol Laboratory, Plant Sciences 
Institute, Beltsville Agricultural Research Center, Beltsville Area, Agricultural Research Service, U.S. Department of 
Agriculture. He is currently with the National Program Staff, ARS, National Agricultural Library, 4th Floor, Beltsville, 


MD 20705. 


Vail is at the USDA-ARS Horticultural Crops Research Laboratory, 2021 South Peach Avenue, Fresno, CA 93727. 


Dix is at the USDA, Forest Service, Forest Health Protection—Washington Office, AB—2S, P.O. Box 96090, 


Washington, DC 20090-6090. 


Nordlund is at the USDA-ARS Biological Control and Mass Rearing Research Unit, Mississippi State, MS 39762. 


Kauffman is at the Animal and USDA Plant Health Inspection Service, Plant Protection and Quarantine, Niles Plant 
Protection Center, 2534 South 11th Street, Niles, MI 49120. 


ABSTRACT 


Coulson, J.R., P.V. Vail, M.E. Dix, et al., eds. 2000. 110 Years of Biological Control Research and Development in 
the United States Department of Agriculture: 1883-1993. U.S. Department of Agriculture, Argricultural Research 
Service. 


Research and implementation of biological control, briefly defined as the use of natural enemies and other benefi- 
cial organisms to control pests, began in North America with the first introduction of an exotic natural enemy in 
late 1883 by the United States Department of Agriculture (USDA). USDA’s biological control programs have 
addressed many agricultural pests and have utilized a variety of natural enemies and antagonists. This report 
provides a brief chronicle of progress in these areas. Many successes have been demonstrated in USDA’s classical 
biological control programs, saving growers more than $2 billion during just the past decade. Considerable 
progress has also been made toward the practical use of augmented insect and nematode natural enemies and in the 
development of pathogens for control of insects and weeds. 


Keywords: agricultural pests, antagonists, arthropod pathogens, arthropods, augmentation, biological control, 
classical, history, competitors, insects, microbial control, mites, natural enemies, nematodes, organism introduc- 
tions, plant pathogens, weeds 


To ensure timely distribution, this report was reproduced as supplied by the authors. It received no publications 
editing and design. The authors’ views are their own and do not necessarily reflect those of the U.S. Department of 
Agriculture. 


Mention of trade names, commercial products, or companies in this publication is solely for the purpose of provid- 
ing specific information and does not imply recommendation or endorsement by the U.S. Department of Agricul- 
ture over others not recommended. 


This publication reports research involving pesticides. It does not contain recommendations for their use nor does it 
imply that uses discussed here have been registered. All uses of pesticides must be registered by appropriate state 
or Federal agencies or both before they can be recommended. 


While supplies last, single copies of this publication can be obtained at no cost from Jack R. Coulson, USDA/ARS/ 
NPS, National Agricultural Library, 4th Floor, Beltsville, MD 20705, or by e-mail from: jcoulson@nal.usda.gov 


Copies of this publication may be purchased from the National Technical Information Service, 5285 Port Royal 
Road, Springfield, VA 22161; telephone (703) 605-6000. 


The U.S. Department of Agriculture (USDA) prohibits discrimination in all its programs and activities on the basis of 
race, color, national origin, sex, religion, age, disability, political beliefs, sexual orientation, and marital or family status. 
(Not all prohibited bases apply to all programs.) Persons with disabilities who require alternative means for 


communication of program information (Braille, large print, audiotape, etc.) should contact USDA’s TARGET Center at 
202-720-2600 (voice and TDD). 


To file a complaint of discrimination, write USDA, Director, Office of Civil Rights, Room 326-W, Whitten Building, 
1400 Independence Avenue, SW, Washington, DC 20250-9410 or call 202-720-5964 (voice or TDD). USDA is an equal 
opportunity provider and employer. 





CONTENTS 


Page 

Acknowledgments and list of contributors and reviewers. ....... 00.0 ccc ce een ete n eens XI 
Piers Be Ata cera yy PS Mek PR PU Ns cee eae hele pee ee sine l 
Peermuon Of “biological control” for this histOry/" 2. We ee ve ee ee D8 l 

Eo ere MC AUP RLICN) i UES ISIN 4G Se ae aa ev eeee dn dv oer enes 3 
SSUMINEE Le BA -k SSR Ne Oe ON Pe ny GA en i URW TE Eis cetacean ebea. 6 
A: Biological control of arthropods (insects, mites and ticks). ........ 00.00. cece eee eee ue 6 
Wr COR TCeY CONMIGO GROMISS iss bie Phe er Ts Be OG VL cee eas 6 

a. Classical biological control (introduction of biological control agents) ........... 6 

b. Augmentation and conservation of biological control agents ................... 9 
eorteroDud-lar matic memannuen es 4h 0h, be OS). OF TR i IE, Bee os oa 10 

PE IEOTION CE OOTIN citi. a ne en es SE se PORES ee Pas 1] 

Eat Ese PION er CCUS Wan © 8 CEPTS wh FA i a OP a oe een 12 
SPeaM ICAL CANIIUE 108- DIANE TOMMOUES 6 iciy eee ts DIYs Poke NV OEE fas aN ges Des 12 
Lye ORICRU CCRIIthn DIAIIT PAINORENS: WG. Ss slvr ee EIEN Gs eee eee ees 13 
SPUMMERCRCRE TR Sod Dk Pe eae EN ed ba TR ee EP IPR Fes coe 15 
A: Biological control of arthropods (insects, mites, and ticks). 1.0.0... 0.00. cece eeu 15 
eS bs SA ca a en a a 15 

a. Classical biological control (introduction of biological control agents) .......... 15 

b. Augmentation and conservation of biological control agents .................. 19 

RPA TEM IM-RIBSITICIERIALOUOS 45.5% i iervlers vcic aoerevinte un Fa SERA ee RET Ree Daviess 19 
PATO PAULINEIIAC UAB ey SPIN eT les Tek seeds ops Acai besa cea 19 
Fae NC MUMSNET YOR WOROR 1 ialxicip tet Palsy urtes Kk area eG ea’ pales sees eee ee 21 

pe Ee aCR CRTLPO! Or THAIND MICTIMIOU OR i KW i cc eee hele scabs pen wneas 21 
PPM SUNITA ECHL) CHLAATIG CALVO a chs areata alate vw a's Te oh xfs whee we a an ee 22 
Chapter H1-/1953-1972- Agricultural'Reseatch Services 10.00 I i cee ands 23 
A: Biological control of arthropods (insects, mites, and ticks). ......... 00.0000 cece eeu 23 

PP ALUROPOG THONORICANCONMO! BUONIS: (fie cS ailiis sia ve hue ee ule ae ee Cd kee ede aes 23 

a. Classical biological control (introduction of biological control agents) .......... 23 

b. Augmentation and conservation of parasites and predators ................... 29 
ae Ey la 33 
OG CRIN ree fd Mas ee Pee Pee reer PEEL EV cca ils 33 

PP i a a a er ee 36 

Ce Bigiogma! comial oP pant nematodesye: 08 1 eee, Oe PG a ae. 39 
Dari ein Loom cr Gland pauiopelis Hse POPU eee ke PIPPI ee e.. 40 


Chapter [V:.1973-1993 - Agricultural Research Service) sear cece ce erent tee ne ee 44 


A: Organizational changes’and general events 7.01 ete eee 44 
B: Biological control of arthropods (insects, mites, and ticks). ...................5.005. 49 
1. Arthropod biological control agents)” Se nteiee en = ieee tee ee 49 
a. Classical biological control (introduction of biological control agents) .......... 49 
b. Augmentation and conservation of parasites and predators .................... 60 
2: Arthropod-parasitic nematodes 0522.52.22) ees = pets eee ear ee cee 66 
3.:Arthropod pathogens svg taeie SEE en te ae geneh eae rsa opel ate cee ee 69 
C: Biological: control ofsweedsigiiiacyne e's res eee 2 ee ee if) 
ly Invertebratenaturalenemiesiot weeds 7253.) tee et nee 73 
2.. Weed. pathogens. «4:38: canna’ secmpetieherw tg raienanct. ho oko am as as aie ae ee 87 
D: Biological control of plant nematodes ees «<5 Herren eee eee eee eee 91 
E: Biological. control.of plant pathogensan |. aitk. acne stil eee oe 92 
Chapter V: 1953-1993 - Forest Service - Overview 24 act ene siete ee 100 
Chapter VI: 1973-1993 - Animal and Plant Health Inspection Service...................... 120 
A: Biological control operations, Plant Protection and Quarantine ..................... 120 
1. Gypsy moth (1963-1979) and cereal leaf beetle (1966-1979) programs ............ 121 
2. Initiation and development of the PPQ biological control implementation 
program (1980-1993 ) scscte So Goris tei ites i ee aia fn oe eee ree 2 121 
B: Methods development, Plant Protection and Quarantine ..................0 0 eee eeee 25 
1; History of methods development]... a... stern cine enone 125 
2. Biological controlactivities 3) ae. oy ae ci- «ee ee eae 126 
3; Acknowledgements iio oc cies nevi sca nes feces ees eel ean reer etree 130 
C: The National Biological Control Institute: —. . )- sensei: ccisien ee ohne 131 
le Establishment of NBC" ooo sce. c's «2 ein Reni eee chee Deere 131 
2. ihe initial missionsfunctions andistatting Of NCI pre a eee ee ee 133 
3. The currentrole.of NBCIv ea uence oe Cee a ae 134 
4. Future of NBCI. 0... itt. fo eee ee eae ee rte an, Berlei erst 135 
Epilogue... ..t:. Sgfattvein Ak. detraghst eapatep ede cd Ree Pee Revere hay eae ne eae ay inet oe 145 


A: Accomplishments and current status of ARS research on classical biological control 


of arthropods and weeds7 a). ec pce ee 3 oye ee ee ee 145 
B: Summary of accomplishments of ARS research on insect control with microbial 
OFBANISMS,.. escape oe sa ale a a's em yee + «alee! Ce ee ee cee ee ee 157, 
ReferenCes” 2. case ea dr beg ark ee sah annie nce (6) agp 0s “ane ae oa ee 166 
Appendix I: Documents cited in;chapter [Vo ge, evaeenet ceepeisineee te 259 
A: Charter of the former ARS working group on natural enemies of insects, weeds, and 
Other pests syiy. 6.0 5:05 se 0 sie ete elee, 2 sutts widens + 9 Ap RI See nae arc umenevi Mue  e 260 
B: Charter of the former USDA work group on biological control agents ................ 264 
C: Memorandum of Agreement between the USDA and California, 1974 revision. ........ 266 
Appendix II: Detailed history of ARS insect pathology research, arranged by location......... 270 
Arizona 
Mesa; Western Vegetable and Sugar Beet Investigations Laboratory ................ 270 
Phoenix; ‘Western Cotton ResearchiLaboratory. ee eee ee 271 
Tucson;Bee Research Uaboratory ye ae ee 273 


vi 


California 


Presno; Horticultural Crops Research Laboratory .0.wsti«.s igi seaie eee. 276 

Riverside.BoydenEntomological Laboratory .. 0.15602 Gino k lan ene soe OER, 281 
Florida 

Gainesville; Medical and Veterinary Entomology Research Laboratory ............. 283 

Orlando; Subtropical Insects Research Laboratory ......5.ci0c0c0sscsreeseeeeers 287 
Georgia 

Tifton; Insect Biology and Population Management Research Laboratory ............ 288 
Illinois 

Peoria; National Center for Agricultural Utilization Research ..................... 289 
lowa 

Anwony (corminseote researer, UN icin aso are date oa one oC es 291 
Kansas 

Manhattan; U.S. Grain Marketing Research Laboratory ................0.00 00000. 292 
Louisiana 

Lake Charles; Gulf Coast Mosquito Research Laboratory ................0.0 0000 293 
Maine 


Orono; Northeast Plant, Soil and Water Laboratory (see Ithaca, New York) 
Maryland 


mee ee Resear. BOGOTA Be siti, arise h + ve Ube Stak AL Ee ds a 296 

Beltsville; Insect Pathology Laboratory/Insect Biocontrol Laboratory ............... 298 
Massachusetts 

Otis ANGB; Gypsy Moth Methods Development Laboratory...................... 306 
Missouri 

Columbia; Biological Control of Insects Research Laboratory ..................... 307 
Montana 

Peete RANSeSiG INSECT ONTO) RESCATCH. —poskarere: peek eeesc Je PES Ns vee ee 311 
New Jersey 

Moorestown; Japanese Beetle Laboratory (see Wooster, Ohio) 
New York 

MACE ain ESOC). LERCATCH: LITE, caice sey rr oan. Lone PO PRUE LAT ee 314 
Ohio 


Wooster; Horticultural Insects Research Laboratory 
South Carolina 

Rotel eee.) Pay CRCIRUIC LADOPAIOLY io avery rer min eects. TRA COE O NGS UU dad ve es 316 
South Dakota 


Brookings; Northern Grain Insects Research Laboratory ........... 00.0000 eeu eae 317 
Texas 

Brownsville: Cotton Insects Research Laboratory) ....ccc een Vere eee cee as 317 

Kerrville; Knipling-Bushland U.S. Livestock Insects Research Laboratory ........... 321 

Py Sas LONG ee GCOL CIs Co tiny Aewr Ae oe? dvi Vireo) SE OR ye BUN cas. 324 
Utah 

Logan; Bee Biology and Systematics Laboratory .... 0.0065. WOME RAN bes rea ee. 324 
Washington 

Yakima; Yakima Agricultural Research Laboratory ............. ccc cece eeecues S27 
Wisconsin 

isdn SUT EG: Pils LADOLRIOTY Fee tale Sie Wiese Aa la PHL is ov ee S21 
Wyoming 

Laramie; Honey Bee Disease Investigations Laboratory ................0.00 eeu 328 
France 

Sévres, Béhoust, and Montpellier; European Parasite Laboratory and European 

PM ACME OC ANTAL Me ania eh 2 wt adi nine dou Coe Ree SMEAR ol. 329 


Vii 


Portugal 


Azores; Japanese Beetle Control Program ..... snes eee eee ewe ees ee ee se 331] 
Litérature cited 3.6.00 LA. aes ee WG ee Oe eet re a eee 332 
Appendix III: Detailed history of biological control in the Forest Service ................... 395 

Ts Preface: sssjcgte Riss as saws @ le ees ele CPR Re ate ANN oh cy nah Teen oC oe oer 395 
Il: Biologicalicontrol of arthropodSiye. = weeny eee aces le ol creer ee B95 
A. Bark beetles.wans4 a eel? Seer Psi nie. eee ee ere 395 
ls Black turpentinesbeetle:. 475 75.7 sycet ee & etc sete sce eae ent ee 395 
2: Douglas-fir beetle Fernnwe's seas Ae ee ia ad ec), See ea 396 
3¢Spruce beetle. :.2.4e ee adie ee Ge ie cate oe 396 
4. Mountain pine beetles vd a. o..028c0h. 2 a. teat ae ee 397 
5 smaller Europeanvelm bark beetles. 32 ene tere ee 401 
6, Southern pine. beetle 2, setae eee tartare) aiatenGoleteise tiers 42, ye 402 
7. Mites and nematodes as natural enemies of bark beetles..................... 404 
B. Shoot and trunk, borers andisheathminersiaary-e aac. same 2s. eo eee 409 
I. Shoot borers:and'sheathininersm er merece ce. ae ae 409 
2. Trunk botersih’: cae Seah LR ee LRT es Pe ee 413 
32 Root. borersee 2s et ets Setar. te Ree re note, ei ee 413 
C. Hardwood defoliatorssirmuc am etree cert eset eee ee oe eens regen ce oe 414 
1. Cottonwood leaf beetle and other chrysomelid beetles ..................005. 414 
2+ Elm Spanworm eres Voges. Se IES a0 neal ae a 415 
3 Fall: cankerwormis e220 eee iat, ee See ee 416 
4. Arthropod parasites and predators of gypsy moth ............. 000 cece ee eeae 416 
5. Development of "Gypchek"™, a gypsy moth pathogen ..................06. 424 
GuSpring cankerworm O00. hoe rae tn me etre. » 427 
TaaW illowesawiltes oi. «..<:+/+: shcisan ee APOE ae Oh) he Oi ee 427 
8. Carge:aspen tortrix@ve ev greens terme. © os ce tes een ee SGC AiS 428 
9. Bacillus: thuringiensis: Agee Au, eet ee), SE ee 428 
D; :Goniter/defoltators. i. sec. eis schist oe eke A ee ane 432 
la Blackheaded pine. sawlly<........12c..,.« Seen nent see ie ae ee 432 
2. Parasites and predators of douglas-fir tussock moth .....................004 433 
3. Douglas-fir tussockimothipathogenss » fueieeyae skein te ae ie 435 
AsEuropean pine 'sawilys.y: sa... oc yee dc wichatwe nee eed ake ele en ee 438 
5: Hemlock defoliators?27..9../.Gi Ve Re a a oe ee 438 
6sIntroduced pine‘sawily” 7.9 ..< Asien sc > ae ue een ne 438 
7. Jack pine.budworm. ... Waseda heed Se ee ee ee 439 
$Larch casebearer™ ew.g cic cece tats Soon aie an ea ee 439 
9. Larch sawfly oi. 3.5:, tyecc.,s SE Ae Re ce ee ee 444 
10, Spruce:budworm/eand: western spruce budworm). tan aster eee 444 
E. Sap-sucking insects) 2. &..-.../ oe fe Pa, Se SE ee eee 453 
I6Balsam woolly adelgidi: . .- Sa0iaee ance ee ee ee 453 
2.."Cypress aphid" +c, ec . Seas See ee ee i 454 
3;-Scales and mealybugs'of pines. ee. ee te 2 455 
lil: Biological control of plant pathogensievaun., svaeese:. eee, 455 
A. Forest diseases «i fin ws Ae eet a. FE EP Re ee ee 455 
1; Biological control of root and butt rots. (eet) eee. ane cee 456 
2. Biological control of stem cankers and other stem diseases .................. 456 
3..Biodlogicalicontrol of vascularwiltstyeige gh eae eens ae 457 
4. Role of host tree resistance to diseases in biological control.................. 457 
5. Futurerends.in-biological:control research}, “es eee ee 458 

B. Mycorrhizal symbiosis 


Vill 


(TOCSY STE 2) ime eT Ue A or gc 463 


See CH EET OND, WOMUS Fo ik, 6 kas wea Ce ea eile Ge eed OUR aye oye wea eee 465 

me ae eeS ECON GE TEEIRE OU gS iw view Geel ass SO ew ae oon he Bien Pia Be 465 

Be ee ae eT A CT TCUPRIIOEE ee yyy aac 4.59 oe var bs Heda R eee 4 Ow WGK Eee va 466 

eee anit ee NE Re Slr oy debs OCA ORT ATTN REVO Vs Oo Mie be eared 467 

Ee Ce ocd ob ORR RU aac Be aie ee or or ea ae a 468 

eee See rm tr ie peas ne vipa ss vbis VP RYN Bin week ges ewes ae 468 

PD UCGCIE LW Ure IN ee en ene IS ee aces oun Vee Gree re ewaee 540 
Indexes 

SOIC E (WORTIZRTIONS AOU MOCNCIOG © Wie ald ions Wie ae ete iat ls Wath 5 lesa 's GM Te oe elec 545 

CUETO T Uo Dee en ee ee ee ee Se ne 560 

A Cu ee men Merete, eles GAN No ids MGs ars ols Se eb el Sele la eee eens 585 

ADIGE INICIE a srcicie oi Pe Oe Ne TO ne ee a ens KEEN GS te EG ee ee oe 635 


TABLES 


Page 

Main Text: 
Table 1. Benefits of some USDA classical biological control programs, 1963-87 .............. 42 
Table 2. Estimated annual savings to farmers and consumers from the alfalfa weevil 

biological control program in the Northeastern United States ....................00000. 43 
Table 3. USDA, Forest Service research and application activities in biological control 

(1953-1993) ssagete a aie Se sis eg, Bh a eite oot ake ePrice ae ee a 108 
Table 4. Pests and associated natural enemies for USDA programs coordinated by the 

Biological Control Laboratories of the Animal and Plant Inspection Service, Plant 

Protection.and Quarantine ¢sciieneeeee Sh wert el pees renee case) ane ae a 137 
Table 5. Chronology of events leading to the establishment of the National Biological Control 

Institute; iigA PHIS iesys oe cps ac Sete re ee ote ea oe ee tere 142 
Table 6. NBCI Customer Advisory Panel members, 1990-92. .............0.00000-20s0e>- 144 
Table 7. Examples of successful classical biological control for which ARS and predecessor 

agencies wereilargely.responsiblen jy ewe ee eee. es eo ee ee 161 


Table 8. ARS scientists devoted full or half time to classical biological control - December, 1993 163 


Table 9. Estimated resources devoted to all types of biological control by the Agricultural 


Research. Service] 98 7ieie xis | bee aetna encase eens ee 164 
Table 10. Estimated scientist-years devoted to all types of biological control in the 
AgriculturabResearch Service:el 987 # gaia (ian eeee rere ce ce ee 165 
Appendix III: 
Table 1. Predators and parasites of the mountain pine beetle in teckel PING ans. ee eee 530 


Table 2. Predator liberations against Adelges piceae (Ratzeburg) in Northeastern United 
States; 1954-1959 nevis: ii Sones rates ee Sqausnciee ised oie ok Teer eae 537 


Table 3. Predators liberated against Adelges piceae (Ratzeburg) in North Carolina, 
1959-1 966 © cet. ots alt ged FRIES fe ie Anas keaten oes id See kegs ee 538 


Table 4. Predators liberated against Adelges piceae (Ratzeburg) in Oregon and Washington, 
1957-1965 


ACKNOWLEDGMENTS 
AND LIST OF CONTRIBUTORS AND REVIEWERS 


This book would not have been possible without the help of many persons, mostly within the 
Agricultural Research Service (ARS), but including scientists from the Forest Service (FS) and 
Animal and Plant Health Inspection Service (APHIS). The authors involved in the main part of this 
book are given in the specific sections, and their affiliations and locations are listed below. The 
names, affiliations and locations of the scientists who reviewed texts of the various sections are also 
listed; since this is a history of USDA research, almost all reviewers were USDA personnel. The help 
of all of these individuals in telling the story of biological control research and implementation in the 
U.S. Department of Agriculture has been, of course, invaluable. Authors and reviewers of 
Appendices II and III, with their affiliations and locations, are given in the respective Appendices, 
along with other acknowledgments. 


Special thanks are due here to three important members of the ARS Biological Control 
Documentation Center: Susan M. Braxton, whose editorial and organizational talents have been 
indispensable in finalization of the text, and who is responsible for preparation of the indexes of this 
book; and Nicole S. Johnson and Glenn W. Hanes, who have painstakingly altered the manuscript to 
meet the editorial requirements of the ARS Information Staff. 


AUTHORS (main text): 
J. R. Adams, ARS, Beltsville, MD (now retired) 

. A. Andres, ARS, Albany, CA (now retired) 

. L. Bruckart, ARS, Frederick, MD 

. Burger, APHIS, Niles, MI (now retired) 
. Carruthers, ARS, Albany, CA 

. Center, ARS, Ft Lauderdale, FL 
. Cook, ARS, Pullman, WA 
. Coulson, ARS, Beltsville, MD 
BE Cunningham, APHIS, Hyattsville, MD 

. H. Day, ARS, Newark, DE 
. Delfosse, APHIS, Hyattsville, MD (now ARS, Beltsville, MD) 
. DeLoach, ARS, Temple, TX 

. Dix, FS, Lincoln, NE (now Washington, DC) 

Hackett, ARS, Beltsville, MD 

BHiowell, ARS, College Station, TX 

. Kauffman, APHIS, Otis AFB, MA (now Niles, MI) 
. King, ARS, Weslaco, TX (now College Station, TX) 
. Kingsley, APHIS, Otis AFB, MA 
indegren, ARS, Fresno, CA 
), Lumsden, ARS, Beltsville, MD 
. Meyerdirk, APHIS, Hyattsville, MD 

. Nickle, ARS, Beltsville, MD (now retired) 

Nordlund, ARS, Weslaco, TX (now Mississippi State, MS) 


Pe ay sate Mee 
2a Rem oe 


OG) 


mee ae ee ee 
oe 


eas 


Xi 


. Papavizas, ARS, Beltsville, MD (now retired) 
. Sayre, ARS, Beltsville, MD (now deceased) 
. Schroeder, ARS, Orlando, FL (now retired) 
erimannin ARS, Beltsville, MD 
. Spurr, ARS, Oxford, NC (now retired) 
. Turner, ARS, Albany, CA (now deceased) 
. Vail, ARS, Fresno, CA 
. Wendel, APHIS, Mission, TX 
C. L. Wilson, ARS, Kearneysville, WV 


mvorTtTEero 
Se 


ae oe 


REVIEWERS: 
Chapters I-IV: 
Sections on Classical Biological Control of Arthropods 
H. A. Cordo, ARS, Hurlingham, Argentina 
W. H. Day, ARS, Newark, DE 
J. J. Drea, ARS, Beltsville, MD (now retired) 
R. J. Dysart, ARS, Sidney, MT (later Montpellier, France, now retired) 
G. T. Fincher, ARS, College Station, TX (now retired) 
R. W. Fuester, ARS, Newark, DE 
L. Knutson, ARS, Montpellier, France (now retired) 
R. W. Pemberton, ARS, Seoul, South Korea (now Ft Lauderdale, FL) 
B. Puttler, ARS, retired (Columbia, MO) 
P. W. Schaefer, ARS, Newark, DE 
Sections on Augmentation of Arthropod Biological Control Agents 
P. D. Greany, ARS, Gainesville, FL 
H. R. Gross, ARS, Tufton, GA (now deceased) 
J.D. Lopez, ARS, College Station, TX 
Sections on Arthropod-Parasitic Nematodes 
(authors only) 
Sections on Arthropod Pathogens 
(in addition to authors) 
M. A. Gilliam, ARS, Tucson, AZ 
L. C. Lewis, ARS, Ames, IA 
Sections on Biological Control of Weeds 
(in addition to authors) 
A. J. Caesar, ARS, Bozeman, MT (now Sidney, MT) 
H. A. Cordo, ARS, Hurlingham, Argentina 
M. A. Jackson, ARS, Peoria, IL 
L. Knutson, ARS, Montpellier, France (now retired) 
P. C. Quimby, Jr., ARS, Bozeman, MT (now Montpellier, France) 
Sections on Biological Control of Plant Nematodes 
(authors only) 
Sections on Biological Control of Plant Pathogens 
(in addition to authors) 
J. A. Lewis, ARS, Beltsville, MD 
Chapter V 
A. T. Drooz, FS, retired (Cary, NC) 
L. G. Eskew, FS, Fort Collins, CO 
G. D. Hertel, FS, Radnor, PA 
D. T. Jennings, FS, retired (Garland, ME) 
D. N. Kinn, FS, Pineville, LA 
N. B. Klopfenstein, FS, Lincoln, NE 


xii 


T. M. ODell, FS, Hamden, CT 
R. C. Reardon, FS, Morgantown, WV 
C. M. Schumann, FS, Lincoln, NE 
T. R. Torgersen, FS, LaGrande, OR 
Chapter VI 
H. W. Browning, University of Florida, Lake Alfred, FL 
R. J. Dysart, ARS, Sidney, MT (later Montpellier, France, now retired) 
N. C. Leppla, APHIS, Hyattsville, MD (now University of Florida, Apopka) 
R. C. MacDonald, North Carolina Dept. Agriculture, Raleigh, NC 
R. G. Van Driesche, University of Massachusetts, Amherst, MA 
Epilogue 
Section A 
W.H. Day, ARS, Newark, DE 
R. W. Fuester, ARS, Newark, DE 
L. Knutson, ARS, Montpellier, France (now retired) 
R. S. Soper, ARS, Beltsville, MD (later Athens, GA, now retired) 
Section B 
M. A. Gilliam, ARS, Tucson, AZ 
L. Knutson, ARS, Montpellier, France (now retired) 


xiii 


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INTRODUCTION 
By J. R. Coulson, D. A. Nordlund, and R. J. Cook 


A. DEFINITION OF "BIOLOGICAL CONTROL" FOR THIS HISTORY 


The subject of this history, as indicated by its title, is biological control. It is important to note, 
however, that the pest management/control community is still working toward a consensus regarding 
exactly what constitutes biological control. There are two basic schools of thought, one arising from 
the field of entomology for control of arthropods and weeds and the other from the field of plant 
pathology for control of microorganisms as plant pathogens. It is also important to note that 
contributors to this publication do not all define biological control in the same way and thus, for the 
purposes of this publication, some boundaries to the definition are needed. 


The entomological tradition supports a limited view of biological control, a term first coined in 1919 
by H. S. Smith, University of California (Smith 1919), and defined by DeBach and Schlinger (1964) 
as: "The actions of parasites, predators and pathogens in maintaining another organism's density at a 
lower average than would occur in their absence." This was not the first definition and there have 
been other more recent ones (Huffaker and Messenger 1976; Coppel and Mertins 1977). It is 
probably the most succinct definition, and restricts biological control to interactions which generally 
involve a density dependent relationship between the biological control agent and the organism being 
controlled. This is an important unifying concept. Under DeBach's definition there is natural 
biological control, which is extremely important in maintaining the populations of many organisms at 
relatively low levels, and applied biological control, which involves active intervention by humans. 


In the plant pathology tradition, the term biological control has been defined (Garrett 1965; Baker 
and Cook 1974) broadly so that any organism (except humans) can be a biological control agent, 
whether the interaction involves a density dependent interaction or not. Somewhat equivalent to 
DeBach's "natural" and "applied" biological control, plant pathologists include both the use of 
practices to enhance or take advantage of "resident antagonists" (actions analogous to "conservation 
of biological control agents" in entomology), and the use of "introduced antagonists" (analogous to 
"augmentation," or more rarely "classical," biological control in entomology). The plant pathological 
concept of biological control includes approaches that lower the population of pathogens, but also 
approaches that arrest or retard disease development or reproduction of the pathogen on or within the 
diseased plant. This tradition led to the recent proposal of a very broad definition for biological 
control: "The use of natural or modified organisms, genes, or gene products to reduce the effects of 
undesirable organisms (pests), and to favor desirable organisms such as crops, trees, animals, and 
beneficial insects and microorganisms" (National Academy of Sciences 1987; Cook 1988). Under 
this definition, naturally occurring interactions as well as a wide range of biologically based pest 
management techniques, including sterile male technique and host resistance, are all considered 
biological control. 


The different approaches to and definition of biological control used in plant pathology compared 
with entomology are not surprising, considering the nature of the agent or process to be controlled 


and the agents used for control. The target is always a plant pathogen, either a fungus, bacterium, or 
virus. The biological control agent is likewise either a fungus, bacterium, or virus. Biological control 
in plant pathology is thus microbe against microbe. The meeting ground between the agent and target 
may be independent of plants, e.g., in soil, but most commonly is on or within plants during the 
disease-producing process. This accounts for the emphasis on interrupting or retarding processes 
such as infection or other events associated with the development of plant disease. In many respects, 
this is analogous to biological control of arthropods, where the control agent is most often another 
arthropod, usually quite unrelated taxonomically to the target, and can also be another invertebrate or 
a microbial pathogen. The meeting ground can also be on or independent of the host organism. But in 
entomology, the emphasis is on reducing the numbers of the target organism and thus the damage to 
the host plant or animal, rather than on limiting a process. 


For the purposes of this history, we will use a definition slightly altered from that used for the U.S. 
Department of Agriculture (USDA), Agricultural Research Service (ARS) biological control 
workshop in 1987 (King et al. 1988): "Use/management of naturally-occurring, introduced, or 
genetically-modified natural enemies (predators, parasites/parasitoids, and pathogens of pests) and 
other selected beneficial organisms (antagonists, competitors, and allelopaths), and their products, to 
regulate populations and effects of pests (invertebrate pests of useful plants, animals, man, terrestrial 
and aquatic weeds, and plant pathogens)." The use of the term "biological control agent" in this paper 
therefore includes both the "natural enemies" and "other beneficial organisms" included in this 
definition. 


The pest management community does not have a shared conceptual model for biological control, 
and thus, some will feel that the definition used here is too broad while others will feel that it is not 
broad enough. Issues, such as the use of dung beetles to destroy fly breeding habitat, which under 
DeBach's definition, would not be considered biological control, will be discussed, and dung beetles 
considered as "biological control agents". Then there are the microbial agents such as the 
endophytes--fungi and bacteria that live in plants--that protect their host plants against certain insect 
pests by production of toxic substances such as alkaloids (Siegel et al. 1987), but without directly or 
necessarily reducing the pest population. These agents do not fit under the categories of parasites, 
predators, or pathogens, but do fit more logically in the plant pathology concept of "antagonists," and 
limiting a "process" (the process by which the pest attacks the plant), and can thus be included in the 
definition used here. On the other hand, host resistance, pheromones, and the sterile male technique, 
which are considered biological control under the broad definition proposed by the National 
Academy of Sciences (NAS) (1987), will not be discussed. The proper definition for "biological 
control" is still being discussed in the scientific literature (Dietrick 1988; Garcia et al. 1988; Gabriel 
and Cook 1990), and may never be entirely resolved. The broader term "biologically based" methods 
of control has been used by USDA-ARS to encompass the use of natural enemies and antagonists as 
well as the many other pest management techniques included in the NAS definition of biological 
control, most recently for a 1993 ARS-sponsored symposium (Lumsden and Vaughn 1993). 


There is a further complication concerning microorganisms, whether for use to control plant 
pathogens, invertebrates, or weeds, that deserves mention here, since definitions are also involved. 
This concerns the different regulatory mechanisms affecting the introduction and development of 
microorganisms as pest control agents, as compared to the introduction and use of invertebrate 
biological control agents. The U.S. Environmental Protection Agency (EPA) considers all organisms 
used for pest control purposes as "pesticides," in accordance with the definitions used in the Federal 
Insecticide, Fungicide and Rodenticide Act (FIFRA). Though the EPA has exempted invertebrate 
organisms (including arthropods and nematodes) from regulation under FIFRA, relying on adequate 
regulation of these organisms by the USDA, microorganisms (including fungi, bacteria, protozoans, 
viruses, and rickettsia) are still regulated by EPA under FIFRA as "microbial pesticides." This 
requires long-term intensive study such as performance trials and safety tests for the introduction and 


2 


use of these organisms as pest control agents, which can include tests originally developed for 
chemical pesticides. This can be a severe deterrent if, as in most cases, development of a commercial 
product is intended, which requires registration by the EPA. The USDA supports research on these 
pest control agents to the point where they can be patented and transferred as a technology to the 
private sector. And the private sector will only further develop and license them for 
commercialization if a profit can be made, which often depends upon a broad target host spectrum 
and high degree of efficacy of the product, and is negatively impacted by the high cost involved in 
the testing and development of the product, caused largely by costs associated with meeting existing 
regulation requirements. As noted in the latter portions of this history, a number of regulatory 
changes are currently being discussed in the EPA and USDA that will affect the introduction and use 
of both invertebrate and microbial biological control agents in the future. 


B. SCOPE AND ORGANIZATION OF THIS HISTORY 


The original intent for the compilation of this history was to help commemorate the first centennial 
anniversary of biological control in the United States, an event celebrated by two international 
symposia in 1989 organized by the University of California and the USDA, and sponsored or 
supported by several other organizations (University of California 1989; U.S. Department of 
Agriculture, Animal and Plant Health Inspection Service, USDA, 1989a). An early draft of this 
history formed the basis for a USDA article relating to this anniversary (Morrison 1989). Though the 
anniversary celebrated the first successful classical biological control program, that is, the 1888-89 
introduction and establishment of the vedalia beetle that controlled the introduced cottony cushion 
scale pest of citrus in California, biological control activities in the USDA began prior to 1888. The 
initiation of USDA biological control research can be considered to have begun in 1883-84 with the 
first successful introduction of an exotic natural enemy to control a pest: the braconid parasite 
Cotesia glomeratus for control of the imported cabbageworm. Though establishment of the natural 
enemy in the United States occurred, this did not result in control of the pest for which it was 
introduced, unlike the case of the vedalia beetle. Also, because of the time required to complete the 
manuscripts for this history, the 1989 centennial date has long since passed. This has resulted in the 
110-year period now covered by this history, which covers events from 1883/84 through 1992/93, 
and includes reference to some literature published in 1994/95. The Epilogue to this History includes 
a discussion of ARS’ classical biological control program with comments on some administrative 
events impacting that program that occurred subsequent to the 1993 cutoff, i.e., 1994-1999. 


The first portions of this history to be completed were those relating to the biological control 
programs of the early USDA bureaus and divisions and of USDA's Agricultural Research Service 
(ARS), following its creation in 1953. Since biological control activities were conducted in other 
USDA agencies, manuscripts were also solicited from the Forest Service (FS) and Animal and Plant 
Health Inspection Service (APHIS). A primary delay in assembling this history was in compiling the 
histories of the Forest Service and ARS insect pathology research. The considerable efforts expended 
and information collected resulted in histories of these two areas in much greater detail than 
compiled for other sections of the overall history. Consequently, these detailed histories have been 
placed in toto as appendices, but they are briefly summarized in the body of the overall history to 
correspond more closely to the treatment accorded other sections. 


This has, however, resulted in a relatively brief history of the early periods and of ARS's biological 
control programs, wherein little mention is made of the many individuals who were involved in the 
early periods and ARS programs, particularly in classical biological control; their contributions can 
be noted primarily by the many literature references cited in those sections that record their work, 
and in the major historical summaries cited (Clausen 1956, 1978; Habeck et al. 1990; Nechols et al. 
1995), and the references cited therein. (Details of some early work on forest insects mentioned in 


Chapters 1 and 2 are given in Appendix III, and more details concerning arthropod pathogens are 
given in Appendix II.) 


Basic research in support of biological control programs is not specifically addressed in this history; 
the demarcation between basic and applied research impacting biological control is often difficult to 
distinguish. 


This is a chronicle of the USDA biological control programs, and little mention is made of the many 
valuable contributions to biological control made by colleagues in other federal and state institutions. 
In particular, the considerable involvement of the University of California in classical biological 
control and in insect pathology from the inception of those disciplines in the United States, and the 
contributions of other institutions such as the Hawaiian Sugar Planter's Association and Hawaiian 
Department of Agriculture, various State Agricultural Experiment Stations and Universities in 
Florida, Massachusetts, Texas, Wisconsin, and many other states, and state agencies in California, 
Colorado, Maryland, Massachusetts, New Jersey, Oregon, Pennsylvania, Virginia, Washington, and 
other states that have been involved in many various aspects of biological control, must be 
acknowledged here. However, little mention of these is made in this history; their contributions are 
discussed in other histories of biological control and in many biological control textbooks cited 
herein (Steinhaus 1946, 1949; Clausen 1956, 1978; Sweetman 1958; DeBach and Schlinger 1964; 
Doutt 1964; Hagen and Franz 1973; Baker and Cook 1974; Huffaker and Messenger 1976; 
Simmonds et al. 1976; Coppel and Mertins 1977; Luck 1981; van den Bosch et al. 1982; Cook and 
Baker 1983; Funasaki et al. 1988; Lashomb et al. 1988; Habeck et al. 1990; Hornby 1990; DeBach 
and Rosen 1991; Stirling 1991; TeBeest 1991; Tjamos et al. 1992; Nechols et al. 1995; and Van 
Driesche and Bellows 1996). 


Much of the research and other activities reported in this publication were conducted by USDA 
scientists in cooperation with state and university colleagues. Histories of two pertinent USDA 
agencies are missing from this compilation -- the Cooperative State Research Service (CSRS) and 
Extension Service (ES); at the end of 1993, these were combined into the new Cooperative State 
Research, Education, and Extension Service (CSREES). The primary function of these agencies has 
been the administration of federal funds that go to the State Agricultural Experiment Stations (SAES) 
and Cooperative Extension Services (CES), respectively, at the land-grant universities throughout the 
United States. In addition, the CSRS/CSREES has provided funds for a number of Regional Research 
Projects that have involved cooperative research between SAES and USDA scientists, including 
several biological control projects. Recent publications of two of those regional projects are 
particularly noteworthy here, recording the results of long-term cooperative SAES/USDA biological 
control research in the Southeastern and Western regions of the United States (Habeck et al. 1990; 
and Nechols et al. 1995, respectively). 


This history of USDA biological control programs is generally organized into four chronological 
periods, 1883/84-1933, 1934-52, 1953-72, and 1973-93. These correspond to four periods initiated by 
major organizational changes in USDA, which have had their impacts, some good, some bad, on 
biological control research and development/implementation programs within the department. The 
history concerns biological control activities of the old Divisions and Bureaus that were combined in 
1952/53 to form ARS. Some units were placed in the Forest Service (FS) at that time. In 1971, 
additional units were removed from ARS to form the Animal and Plant Health Inspection Service 


(APHIS). Reviews of biological control activities in the latter two USDA agencies are included in 
this history. 


Within each of the four main historical periods, the history of early studies and ARS research is 
further organized by the agricultural pests targeted for biological control, i.e., arthropods (insects, 


mites, and ticks), weeds, plant nematodes, and plant pathogens. And finally, the sections on 


4 


arthropod pests are further organized by the type of natural enemy or other organism used for control, 
i.e., arthropod parasites (parasitoids) and predators, arthropod-parasitic nematodes, and arthropod 


pathogens. The last section on weeds is similarly organized by natural enemy, i.e., invertebrate weed 
feeders and weed pathogens. 


The sections on Forest Service and APHIS are differently organized, in accordance with the 
treatments preferred by their authors and editors, and are general overviews of biological control 
activities in those two agencies. As noted above, detailed treatment of the Forest Service activities 
appears as an Appendix. 


Included in the Indexes to this history are all scientific and common names of pest and beneficial 
organisms mentioned in the text of the main body and appendices, cross-referenced and with 
reference to the higher taxa to which the organisms belong. Common names of arthropods not 
approved by the Entomological Society of America (ESA) (Stoetzel 1989) appear in quotes in the 
text. Other texts used in compiling the Indexes are mentioned therein. 


CHAPTER I 
1883-1933 


A. BIOLOGICAL CONTROL OF ARTHROPODS (INSECTS, MITES, AND TICKS) 
1. Arthropod Biological Control Agents 
a. Classical biological control (introduction of biological control agents). By J. R. Coulson 


During the early years of the U.S. Patent Office's Bureau of Agriculture (1853-62) and its successor 
the Department of Agriculture (USDA, 1862-81), the several bureau and department entomologists 
(T. Glover, 1853-59 and 1862-78; C. V. Riley, 1878-79; and J. H. Comstock, 1879-81) published 
observations on natural enemies of agricultural pests. Concurrent observations were being made by 
several State Entomologists, some of whom (A. Fitch, New York; B. Walsh, Illinois) suggested the 
importation of parasites of introduced pests. Some of the State Entomologists (C. V. Riley, then 
Missouri State Entomologist; and W. LeBaron, Illinois State Entomologist) began within-state 
redistribution of parasites in the 1870s. Riley made the very first international shipment of an insect 
natural enemy in 1873, sending specimens of a predaceous mite to France to control the grape 
phylloxera. (Riley 1893; Doutt 1964; Rainwater and Parencia 1981.) 


It was not until the establishment of the Division of Entomology in 1881 under its Chief, C. V. Riley, 
that the USDA initiated research on what is now known as classical biological control. Riley 
arranged the first importation and establishment of an insect parasite in the U.S. (District of 
Columbia, lowa, Nebraska and Missouri) in 1883-84, the braconid Cotesia glomeratus, a European 
parasite of the imported cabbageworm. He was also responsible for the highly successful importation 
of the so-called vedalia beetle, Rodolia cardinalis, from Australia in 1888-89 into California for the 
control of the cottony cushion scale, Jcerya purchasi. This scale had become a severe threat to the 
infant California citrus industry. The vedalia beetle quickly became established in California. By the 
end of 1889 it had caused a spectacular decline in scale populations there. Oddly enough, Riley had 
been forced to resort to a subterfuge of sorts to obtain from the U.S. Congress the necessary funds 
($2,000) to support the foreign travel of a USDA entomologist (A. Koebele) to Australia for 
collection of natural enemies of the scale. (Riley 1893; Doutt 1958, 1964; Clausen 1956, 1978; 
Caltagirone and Doutt 1989.) 


The spectacular success of the vedalia beetle led to a rapid expansion of introductions and other use 
of natural enemies in California, and also in Hawaii. Other than financing of one further exploration 
in Australia by Koebele, the USDA played little part in biological control during Riley's remaining 
years as the Division Chief (he served as Chief during 1881-1894), and even in the very early years 
of his successor, L. O. Howard, Chief of the Division of Entomology, 1894-1904 (and later of the 
Bureau of Entomology, 1904-27). 


In fact, the relationship between the USDA and the California programs became strained, primarily 
due to Howard's concerns about possible placement of too much emphasis on importation of natural 


enemies at the expense of other pest control measures in California and a perceived reckless handling 


6 


of importations. These concerns were eased at the passage of the Federal Plant Quarantine Act in 
1912, and appointment in 1913 of H.S. Smith, a former USDA entomologist, as superintendant of the 
state insectary at Sacramento (built in 1907). With this appointment, Smith was thus placed in charge 
of California's natural enemy importations; he was made an official collaborator of the USDA. In 
1931, the California biological control importation program was formalized under a three-way 
Memorandum of Agreement involving USDA, University of California, and the California 
Department of Agriculture. This ongoing agreement has been updated and renewed several times (for 
the most recent draft, see Appendix I.C), and sets forth procedures to be followed and certain 
applicable restrictions in regard to the USDA and University programs in California. (Clausen 1956; 
Doutt 1964; Hagen and Franz 1973; Simmonds et al. 1976; Rainwater and Parencia 1981.) 


While the natural enemy importation programs in the states of California and Hawaii quickly 
expanded, early USDA importations were limited to a few natural enemies of the Hessian fly from 
England (1890-94), San Jose and white peach scales from Japan and China (1895-96, 1901-02), 
barnacle and Florida wax scales from Italy (1895-98), and boll weevil from Guatemala (1904). With 
the exception of the Guatemalan predator of the boll weevil, which was brought directly to Texas, 
these shipments were initially received at the insectary at division headquarters in Washington, DC. 
From there they were disseminated to division entomologists in Louisiana (for barnacle and wax 
scales) and several eastern and midwestern states. Two of the predators and one parasite were 
established, but with little effect on the pests. (Clausen 1956, 1978.) 


In 1905, USDA began its first large-scale biological control program, embarking on explorations in 
Europe and to a lesser extent Japan for natural enemies of the gypsy moth and browntail moth. These 
two introduced pests had become severe pests of forest and other trees in Massachusetts and other 
areas of New England. Importations and releases of natural enemies, first begun in cooperation with 
the State of Massachusetts (1905-11), were made during 1906-14 and 1921-33. Explorations were 
conducted by USDA entomologists of the Bureau of Entomology's Division of Forest Insect 
Investigations (or variously Gipsy Moth and Brown-tail Moth Investigations). Shipments were 
received at the Bureau's newly established Gypsy Moth Laboratory at Melrose Highlands, MA, for 
emergence, identification, culture, and dissemination of the natural enemies. The program resulted in 
the establishment of nine species of parasites of the gypsy moth, seven of the browntail moth, and 
two predators of both moths. Although the introduced natural enemies contributed to limiting 
populations of the gypsy moth, continuous economic control of this pest was not achieved. However, 
substantial control of the gypsy moth at least in New England can be claimed, since outbreaks there 
were reduced in frequency, duration, and severity. Such population suppression appears to have 
spread into areas more recently invaded by the gypsy moth. In addition, the established browntail 
moth parasites, along with others introduced later in connection with the satin moth program, are 
generally considered to be the major factor in controlling the browntail moth in New England. 


Many basic biological control concepts, principles, and procedures were developed as a result of this 
program, which involved a number of state and USDA entomologists who were later to become key 
personnel in the USDA and California biological control programs. (Howard and Fiske 1911; 
Burgess and Crossman 1929; Clausen 1956, 1978; Dowden 1962; Hagen and Franz 1973; Elkinton 
and Liebhold 1990; Williams et al. 1990, 1992, 1993; Berryman 1991.) 


During 1905-18, the Bureau of Entomology imported parasites and predators of the elm leaf beetle 
(from Europe, 1907-08 and 1917), citrus whitefly (from India, 1910-11), alfalfa and clover leaf 
weevils (from Europe, 1911-13), and sugarcane borer (from Cuba, 1915), and transferred (without 
success) some of the established gypsy moth natural enemies from New England to New Mexico in 
an attempt to control the range caterpillar. The alfalfa weevil program was USDA's second major 
importation program, and resulted in the establishment of several species of parasites in Utah where 
this European weevil had been recently introduced accidentally. The most important parasite 


subsequently dispersed widely with the weevil in western states. A parasite of the clover leaf weevil, 
an earlier introduced pest, was also established, in the eastern U.S., as an incidental result of this 
program. There were mixed results from the other programs, with some establishments but little 
economic control. (Chamberlin 1924; Clausen 1956, 1978.) 


An important event occurred in 1919 with the founding of a USDA laboratory in Europe. This 
laboratory was established at Auch in southern France by W.R. Thompson of the Bureau of 
Entomology's Division of Cereal and Forage Insects Investigations for the conduct of the large-scale 
European corn borer program initiated that year (and which continued through 1938). The European 
corn borer was first discovered in the U.S. in 1917 and quickly became a major pest. Shipments of 
natural enemies were made initially directly to the Bureau's European Corn Borer Laboratory at 
Arlington, MA. Of 24 parasite species imported, six became established in the U.S. but failed to 
provide satisfactory control of the borer. Additional studies in Europe were made at the laboratory in 
France on natural enemies of the alfalfa weevil (1921-28), European earwig (for Oregon, 1924-31), 
and peach twig borer (for California, 1931), resulting in establishment of additional parasite species 
in the U.S. From 1922 until his retirement in 1960, H.L. Parker was in charge of the USDA 
laboratory in Europe, soon to be known as the European Parasite Laboratory. This Laboratory has 
been moved to several locations in France (and to South America, see Chapter IT) throughout its 
existence, the last being at Béhoust, near Paris, prior to its consolidation with the ARS Rome 
laboratory at Montpellier to become the European Biological Control Laboratory in 1991 (see 
Chapter IV). (Baker et al. 1949; Drea 1981.) 


A second USDA overseas laboratory was established by the Bureau's Division of Deciduous Fruit 
and Shade Tree Insects Investigations in Japan by 1922. Explorations were conducted from this and 
other oriental field stations in Japan, Korea, and China for natural enemies of Japanese beetle 
(1920-33), gypsy moth (1921-22), oriental beetle (1925-26 and 1932), Asiatic garden beetle 
(1927-34), oriental moth (1929-30), European corn borer (1929-36), and oriental fruit moth 
(1929-39). These oriental field stations were consolidated into one laboratory at Yokohama, Japan, in 
1932, under the leadership of G.J. Haeussler (1932-34), later to be called the Asian Parasite 
Laboratory (see Chapter IT). (Clausen et al. 1927; Allen et al. 1940; Haeussler 1940; Gardner and 
Parker 1940; Clausen 1956, 1978.) 


Another USDA overseas laboratory was established in Hungary in 1926 as the Gypsy Moth 
Laboratory, later Central European Investigations, by R.T. Webber and C.F.W. Muesebeck of the 
Bureau's Division of Forest Insect Investigations. Projects conducted there, in addition to that on 
gypsy moth, included those on satin moth (1927-34), "birch leafmining sawfly", Heterarthrus 
nemoratus (1930-34), European pine shoot moth (1931-1934), larch casebearer (1932-34), and some 
exploratory work on the beech scale. (Burgess and Crossman 1929; Dowden and Berry 1938; 
Clausen 1956, 1978.) Another foreign laboratory was established in 1928 in Mexico by A.C. Baker 
of the Bureau's Division of Insects Affecting Fruit and Shade Trees, to study insect pests of tropical 


and subtropical crops and ornamentals, including fruit flies. (McPhail and Bliss 1933; Baker et al. 
1944.) 


Other importations made by USDA during the remaining tour of duty of L.O. Howard and of his 
successor C.L. Marlatt, Bureau Chief from 1927-1933, included natural enemies of Mexican bean 
beetle from Mexico (1922-23 and 1929-30), sugarcane borer from South America (1928-32), and the 
gray sugarcane mealybug from Hawaii (1932). Also, explorations for natural enemies of the beet 
leafhopper were begun (1926-28), natural enemies of citrus blackfly were introduced into Cuba from 
Malaya (1930), a native parasite of the Nantucket pine tip moth from Virginia was successfully 
established in Nebraska, and a native parasite of the woolly apple aphid was successfully recolonzied 
from the eastern to northwestern U.S. (1930-31) and subsequently to several other countries. 


(Clausen and Berry 1932; Baumhofer 1932; Jaynes 1933; Landis and Howard 1940; Clausen 1956, 
1978.) 


Significant accomplishments of USDA's classical biological control programs during 1883-1933 
included not only the development of concepts, procedures, and principles of biological control, and 
the training of numerous scientists in this new field of pest management, but also the establishment 
of numerous parasites and predators of many of the introduced insect pests in the U.S. Some of these 
have contributed to the substantial or appreciable suppression of economic populations of such pests 
as the oriental, satin, browntail, and gypsy moths in New England and the alfalfa weevil in large 
areas of western U.S., and at least partial suppression of populations of sugarcane borer in Florida, 
European corn borer and Japanese beetle in eastern U.S., and the European earwig in the Northwest. 
Complete control of the cottony cushion scale in California and citrus blackfly in Cuba was obtained. 
In addition, movement of native parasites from eastern U.S. caused substantial control of the western 
pine tip moth in Nebraska and the woolly apple aphid in northwestern U.S. and in several foreign 
countries. Many other insect pests are reported to have been completely, substantially, or partially 
controlled as a result of the state and university biological control programs in California and Hawaii 
during this period. (DeBach 1964; Laing and Hamai 1976; Luck 1981; and DeBach and Rosen 1991.) 


The intense interest in biological control generated by the successful cottony cushion scale control 
began to wane during the latter part of this early period. A count of research papers shows that the 
ratio of those devoted to biological control research versus those related to insecticide research 
shifted from a 1:1 ratio in 1915 to 0.3:1 in 1925, the beginning of a trend that continued into the 
1940s (Sailer 1973), and perhaps reflected disappointment in the results of the USDA biological 
control program, despite the substantial achievements noted above. L.O. Howard warned of over 
expectations for biological control, while also warning of too easy discouragment, in a paper setting 
forth his assessment of the USDA and other biological control programs shortly before his retirement 
(Howard 1926). 


b. Augmentation and conservation of arthropod biological control agents. By D. A. Nordlund, J. R. 
Coulson, and E. G. King 


Augmentation is an approach to applied biological control that involves actions taken to increase 
populations of, or beneficial effects of biological control agents (Rabb et al. 1976; DeBach and 
Hagen 1964; Ridgway and Vinson 1977). This approach may involve indigenous or introduced 
biological control agents. There are two basic strategies for augmentation: periodic release and 
environmental manipulation. 


Periodic releases of the biological control agent is the approach to augmentation that has received the 
most attention. Periodic releases may be inoculative or inundative and may involve field-collected or 
laboratory- reared organisms. Inoculative releases involve a relatively small number of the biological 
control agents and depend on the progeny of the released organisms to suppress the pest population 
(DeBach and Hagen 1964). Inoculative releases, for example, are appropriate for the reintroduction 
of a biological control agent into an area in which it cannot overwinter, but is effective during the 
growing season. Inundative releases, on the other hand, involve releases of relatively large numbers 
of the biological control agent and depend on the actions of the released individuals for pest 
suppression (DeBach and Hagen 1964; Flanders 1930, 1951; Stinner 1977). These releases require 
large-scale cultures of the biological control agent. They are intended to provide a relatively rapid 
suppression of the pest population, but are not expected to provide any continuing population 
suppression. Thus, inundative releases are repeated on an as-needed basis throughout the growing 
season. 


Environmental manipulation is the second approach to augmentation. One of the earliest known 
examples of environmental manipulation to increase the effectiveness of a predator is the practice in 
China, by 300 AD, of constructing bamboo runways to provide predatory ants easy transit from one 
pest-infested citrus tree to another (Flint and van den Bosch 1981). Environmental manipulation can 
take a variety of forms and is differentiated from cultural controls in that its direct effect is intended 
to be on the biological control agent, not on the pest. 


"Conservation" is an approach to applied biological control that involves actions taken to protect or 
maintain existing populations of biological control agents (van den Bosch and Telford 1964; Rabb et 
al. 1976). In practice, this means not taking actions that have a negative impact on the populations of 
biological control agents (Nordlund 1984). It can be difficult to differentiate between augmentation 
and conservation. Thus, Nordlund (1984) suggested dropping this terminology and simply using 
periodic release and environmental manipulation. However, the augmentation and conservation 
terminology is still in general use. 


The reality is that applied biological control usually involves a variety of approaches. When 
conducting a release program, whether classical importation or augmentation, it is necessary to avoid 
actions that have a negative effect on the population of biological control agents. Thus, conservation 
should always be an important aspect of biological control. In addition, environmental manipulation, 
to improve the effectiveness of a release program (or biological control agents that have been 
conserved), is also important. These various divisions are designed to assist in our communication, 
but are not generally expected to be exclusive and stand alone biological control approaches. 


Early large-scale augmentation attempts, including those by the USDA to control the boll weevil 
(1906-07) and house flies (1914) in Texas, and by the University of Kansas to control the greenbug 
(1907), utilized native parasites (Pierce 1908; Clausen 1956). These were the forerunners of 
subsequent release programs utilizing the native Hippodamia ladybug for aphid control in vegetables 
in California from 1910, the introduced predator Cryptolaemus against mealybugs in California from 
1910, and the native parasite Macrocentrus ancylivorus against the introduced oriental fruit moth by 
the USDA and several states in many areas of the U.S. from 1929. Other early USDA augmentation 
programs included the use of a native egg parasite against the range caterpillar in New Mexico 
(1930-32), Trichogramma species against the pecan nut casebearer in Georgia (1931) and the oriental 
fruit moth in New Jersey (1930-31), and large-scale culture and release of an imported tachinid 
parasite of the Mexican bean beetle (1930-1935) that involved releases in 19 states. Augmentation 
received an important boost with the development of mass rearing techniques for Trichogramma egg 
parasites by University of California researchers by 1930. (Flanders 1930; Allen and Warren 1932; 
Clausen 1956.) 


The history of USDA research and implementation of environmental manipulation and conservation 
programs in biological control is difficult to compile, since research results appear in papers that are 
not usually indexed to these subjects, and are thus difficult to identify. But these approaches are once 
again becoming important as many of the chemicals once used for pest control are being banned for 
use in many agricultural systems. 


2. Arthropod-Parasitic Nematodes. By J. R. Coulson and W. R. Nickle 


Although a number of observations of plant nematode problems in agriculture had been made by 
USDA scientists, a major role in the development of the science of nematology was to be played by 
N. A. Cobb, known as the "father of nematology" in the U.S. Cobb was hired by the USDA in 1907, 
serving first in the Office of Agricultural Technology in USDA's Bureau of Plant Industry, where he 
continued his studies on nematodes and plant pathology, which eventually led to the formation in the 


10 


1920s of the Nematology Investigations, later the Division of Nematology, within that Bureau, with 
Cobb serving as the Division's first Chief until his death in 1932. 


Early work on the taxonomy and biology of insect-parasitic nematodes was conducted for the most 
part in Europe. However, among American scientists who first recognized the potential use of 
nematodes as biological control agents of insects were the leaders of USDA's Division of 
Nematology, beginning with Cobb, based on his experience with three entomophilic nematodes 
(Cobb 1927). G. Steiner and J. R. Christie joined Cobb at the USDA farm in Washington, DC, and 
produced a long series of papers on insect nematology. Their work on Agamermis decaudata, a 
nematode parasite of grasshoppers and other insects, is considered a classic (Cobb et al. 1923). 
However, the advent of the Japanese beetle research in the 1920s, and the discovery of nematodes 
attacking this pest, resulted in more intensive research on the potential biological control of insects 
by nematodes, in the early 1930s. This early work on an apparently indigenous nematode described 
by the USDA taxonomist, Steiner, was conducted by the New Jersey Department of Agriculture in 
cooperation with the USDA Japanese beetle program in New Jersey. Thus, during this early period, 
most of the nematology research effort in the USDA was centered around insect-parasitic nematodes. 
After Cobb's death in 1932, Steiner became head of the Division of Nematology (1932-56) and the 
emphasis moved to research on plant nematodes, though Steiner continued studies on the taxonomy 
of mermithids, an important insect-parasitic group of nematodes. See also Section C below on 
biological control of plant nematodes. (Clausen 1956; Fleming 1968; Dowler and Van Gundy 1984; 
Nickle and Welch 1984.) 


3. Arthropod Pathogens. By J. R. Coulson, H. Shimanuki, and P. V. Vail 


As in the case with insect-parasitic nematodes, early studies on insect pathogens and their use in 
control of pests took place in Europe (Steinhaus 1964). As noted by Steinhaus (1949), in order for 
insect pathology/microbial control to develop as a distinct discipline, separate projects dealing solely 
with this subject were needed. Two such projects, the study of the diseases of the honey bee and their 
control and, later, in 1922, an extensive program on pathogens of the newly introduced Japanese 
beetle, were initiated by the USDA. Many of the early studies relied heavily on surveys and were 
descriptive in nature. However, the studies by G. F. White (1906-1920) noted below provided the 
basis of understanding of the foulbroods and also therapeutic measures for these and other bee 
diseases. Intensive programs on bee diseases continue to this day. 


Though there were some early attempts made by USDA entomologists to use pathogens for control 
of insect pests, insect pathology research in the USDA essentially began in the Bureau of 
Entomology's Division of Bee Culture Laboratory at Somerset, MD, in 1905. Research on honey bee 
diseases was conducted there under E. F. Phillips, leader of the Investigations, 1906-24 (Phillips 
1906, 1908). He was joined at Somerset by G. F. White in 1907 and in 1916 by A. P. Sturtevant, who 
was transferred in 1926 to the Investigations' Field Laboratory at Laramie, WY. It was Phillips, 
writing in the preface of White's 1906 publication, who differentiated and named American 
foulbrood and European foulbrood diseases of bees. Subsequently, White and Sturtevant published 
several papers on these and other diseases of the honey bee (White 1906, 1907, 1912, 1919, 1920; 
Sturtevant 1932, 1936). 


The early studies by USDA personnel on the use of pathogens for control of insect pests included: 
(1) dissemination of diseased chinch bugs infected with a native fungus pathogen in Minnesota and 
Kansas, 1888-96 (Billings and Glenn 1911); (2) introduction of fungal pathogens of grasshoppers 
imported from South Africa in 24 states, 1900 (Howard 1902); (3) experiments with apparently 
native fungi of the browntail moth in New England, 1908-11 (Speare and Colley 1912) and of the 
citrus whitefly in Florida, 1910-11 (Morrill and Back 1912); and (4) studies of fungal pathogens of 
the gypsy moth imported from Japan, 1910 (Speare and Colley 1912) and of the European corn borer 


1] 


imported from China, 1931-32 (Bartlett and Lefebvre 1934). The Japanese fungal pathogen of gypsy 
moth, later described as Entomophaga maimaiga, was reintroduced in the 1980s, and has proven to 
be an effective control agent; see Chapter IVB3 and Appendix II. A virus disease of the gypsy moth, 
apparently introduced during the gypsy moth biological control importation program, first appeared 
in New England in 1907, and assumed epidemic proportions in heavy gypsy moth populations 
(Glaser 1915). But the first intentional attempts to utilize insect viruses for insect control in the U.S. 
did not take place until many years later. The lack of a concerted effort on pathogens, either native or 
introduced, was noteworthy. 


A major impetus in U.S. research on use of insect pathogens occurred as a result of the Japanese 
beetle program, when the bacterial milky spore or milky disease of this pest was discovered in New 
Jersey in 1933; G. F. White had just been transferred to the Japanese beetle laboratory in New Jersey, 
and was involved in the identification of the organism (Hawley and White 1935). Research efforts at 
Moorestown, NJ, on the Japanese beetle were intensified with the work of G. E. Spencer, R. W. 
Glaser, and H. Fox, and expanded in the 1930s to include White, I. M. Hawley, and S. R. Dutky. This 
early work evolved into extensive studies on all aspects of the use of the "milky disease" organism(s) 
as microbial agents. Use of the "milky disease" bacterium to control Japanese beetle continues today, 
as does research to further understand and utilize this organism. The importance of this pathogen for 
control of the Japanese beetle has been discussed by Steinhaus (1949, 1964), Clausen (1956), 
Fleming (1968), and Cameron (1973), and a bibliography of the bacteria was prepared by Klein at al. 
(1976). 


B. BIOLOGICAL CONTROL OF WEEDS. By J. R. Coulson 


Credit for initiation of biological control of weeds in the U.S. goes to the Hawaiian Sugar Planter's 
Association, which financed the collection in Mexico of natural enemies of lantana, an introduced 
weedy plant in Hawaii, for shipment and release in Hawaii in 1902. Though biological control of 
weeds quickly developed in other areas of the world, it was not until the 1940s that such research 
was conducted in the continental U.S., first by the University of California, 1940-42, and beginning 
in 1944 by the USDA in cooperation with the University of California. (See Goeden, 1978.) 


C. BIOLOGICAL CONTROL OF PLANT NEMATODES. By R. M. Sayre and J. R. Coulson 


The first natural enemy of nematodes, a nematode-trapping fungus, was discovered in the mid-1800s, 
and additional natural enemies were discovered in the early 1900s. Interest in use of these to control 
plant-parasitic nematodes developed early, and greenhouse tests were conducted, but no field tests 
were done. Again, N. A. Cobb and other nematologists of USDA's Nematology Investigations (later 
Division) of the Bureau of Plant Industry played a major role in this research (see the Section A.2 
above on insect-parasitic nematodes for notes on the early history of insect nematology in the U.S.). 
Interest waned when low-cost nematicides became available in the 1940s, but began again in the 
1970s when use of these nematicides were being lost due to actions by the Environmental Protection 
Agency (EPA). Knowledge of natural enemies of nematodes is still inadequate and there are still 
very few nematologists involved in research on biological control of plant-parasitic nematodes in the 
U.S. (Sayre 1971, 1988; Mankau 1973, 1980; Kerry 1981; Smart 1986.) 


In the year 1889, the beginning of this historical survey, N. A. Cobb, founder of the science of 
nematology in the U.S., had just received his doctorate from the University of Jena. It was some two 
years after his appointment to the USDA in 1907 that he succeeded in adding to his assigned studies 
investigations on nematodes. Even then, it would be another decade before he was to propose that 
predaceous soil nematodes might serve as agents for the biological control of plant-parasitic 
nematodes (Cobb 1920). G. Thorne, J. R. Christie, W. E. Chambers, E. G. Titus, and G. Steiner, who 
joined the USDA Nematology Investigations early, were trained or greatly influenced by Cobb. (As 


12 


an example, Steiner was also to propose that Mononchus nematodes, through their predaceous habits, 
were bioregulators of plant-parasitic nematode populations [Steiner and Heinly 1922].) 
Consequently, like Cobb, each was a keen observer of the morphology of healthy nematodes and 
recognized parasites and predators present in nematode samples. They incorporated information on 
the antagonists of nematodes into taxonomic descriptions of new nematode species. This practice 
resulted in a body of information on natural enemies of nematodes being scattered throughout the 
taxonomic literature (Thorne 1961). The first attempt to bring together all the literature on parasites 
of nematodes was not until 1946 (Dollfus 1946) and the next was over 40 years later (Poinar and 
Jansson 1988). 


Some of these early investigators even recognized the occurrence of natural crashes in the 
populations of plant nematodes, and attributed the declines to one or more of the associated 
antagonists. Generally, most investigators did not subject their conjectures on population declines to 
any further rigorous tests either in greenhouse or field plot studies. Perhaps the effort by Thorne 
(1927) to show the economic importance of Mononchus species came the closest to good 
documentation of a biological agent for control of the beet cyst nematode (though he cast doubt on 
whether biological control of the nematode was possible under the soil conditions of Utah). 


In this same 1927 paper, Thorne also discussed and illustrated a "sporozoan" parasite of nematodes 
that he later described as Duboscqia penetrans (Thorne 1940). The species was transferred first to 
genus Bacillus (Mankau 1975) and later to Pasteuria (Starr and Sayre 1985). Starr and Sayre (1988) 
redefined P. penetrans as limited to attacking root-knot nematodes and described a sibling species, P. 
thornei, attacking root-lesion nematodes. 


At the end of this early period, upon the death of Cobb in 1932, Steiner assumed leadership of 
USDA's Division of Nematology. He served in that capacity until 1956. 


D. BIOLOGICAL CONTROL OF PLANT PATHOGENS. By R. J. Cook 


Much of the effort on the biological control of plant pathogens during 1889-1933 was made by state, 
university, and foreign scientists, though USDA scientists made key contributions during this period. 
However, most of the more intensive research in this field has occurred only in recent years. (Cook 
1981; Cook and Baker 1983; Baker 1987; Hornby 1990.) 


The first reference to biological control in plant pathology literature was made by a German plant 
pathologist, C. F. von Tubeuf, in 1914. It was only seven years later that C. Hartley, of USDA's 
Bureau of Plant Industry, Office of Investigations in Forest Pathology, made the first attempt at direct 
introduction of microorganisms into soil for biological control of a plant pathogen (Hartley 1921). 
He tested 12 fungi and one bacterial strain in steamed nursery soil for their antagonistic potential 
against damping-off of pine seedlings caused by Pythium debaryanum. Significantly less 
damping-off occurred in the treated soil compared with the same soil without the introduced fungi. 
Hartley's report was followed by papers by scientists in the United Kingdom and Canada reporting 
successful control of common scab of potatoes and take-all of wheat in sterilized soil by antagonistic 
fungi or bacteria introduced into such soils (Millard and Taylor 1927; Sanford and Broadfoot 1931; 
Henry 1931; Baker 1987; Cook 1988). 


Soil steaming and fumigation have been used extensively in nurseries, greenhouse beds, and open 
fields since Hartley's classic work, but nearly 50 years passed before microorganisms would again be 
tested for their potential to enhance or extend the control of soilborne pathogens provided by these 
heat or chemical treatments. 


Except for the work by Hartley, there are no published reports of USDA plant pathologists having 
attempted to control either fungal or bacterial diseases with introduced antagonists during this early 
period. The emphasis instead was on collection and release of genes for resistance to plant diseases. 
While entomologists were exploring the original homes of naturalized insect pests and collecting and 
importing their natural enemies, USDA plant pathologists, cooperating with plant geneticists, were 
exploring the original homes of plant pathogens to collect germplasm of the plant hosts as a source of 
resistant genes for deployment in U.S. crops. 


During these same early years, plant pathologists attempted the approach used by entomologists, with 
emphasis on antibiotic-producing fungi introduced into raw soil for biological control of root 
pathogens, since there was a general lack of resistance genes for defense against fungal root 
pathogens. It was learned early, however, that raw soil has remarkable resiliency against the 
introduction of alien microorganisms or the establishment of native organisms at populations above 
natural levels. Indeed, these early attempts were so consistently unsuccessful that all further efforts 
along these lines would be abandoned for the next 50 years. 


In 1929, H. H. McKinney of the USDA Bureau of Plant Industry, reported the results of his research 
on inoculation of tobacco plants with various mixtures of mild and severe strains of the "green 
mosaic" and "yellow mosaic" viruses, and showed that plants first inoculated with one virus were 
protected from infection of another closely related virus or a mild strain of the same virus 
(McKinney, 1929). Thus became known the phenomenon of "cross protection," which has been 
shown to have general applicability for most, if not all, major groups of plant viruses. This approach 
to biological control of plant viruses, i.e., inoculating plants with a mild strain to protect them for 
part of their productive life against a severe strain of the virus, is now used on nearly every continent. 
US. plant virologists have studied cross protection extensively in the laboratory since McKinney's 
discovery, but consider its use as a last resort because of risk that a mild virus of one crop could be 
severe or act synergistically with other viruses in other crops. This problem may now be overcome as 
a result of recent discoveries discussed later in this history. 


14 


CHAPTER II 
1934-1952 


A. BIOLOGICAL CONTROL OF ARTHROPODS (INSECTS, MITES, AND TICKS) 
1. Arthropod Biological Control Agents 
a. Classical biological control (introduction of biological control agents). By J. R. Coulson 


Until 1934, all USDA foreign explorations and introductions and releases of natural enemies and 
other biological control agents were handled independently by the various commodity-oriented 
Investigations (or Divisions) of the Bureau of Entomology. In 1934, the Bureau of Entomology was 
combined with the old Bureau of Plant Quarantine to form the Bureau of Entomology and Plant 
Quarantine (BEPQ). Chiefs of this new Bureau were L. A. Strong (1934-41), P. N. Annand 
(1941-50), and A. S. Hoyt (1950-53). Within this new Bureau, there was formed in 1934 a Division 
of Foreign Parasite Introduction, which was charged with the responsibility for all Bureau 
exploration for, and importation of, foreign insect parasites and predators and their distribution to the 
various other Bureau Divisions for utilization in their biological control programs. This was the first 
agency in the USDA providing centralized direction of natural enemy introductions, and such an 
agency, under various names, continued until 1972. (Clausen 1956; Rainwater and Parencia 1981.) 


The Division was placed under the direction of C. P. Clausen, who continued in that position until 
his retirement in 1951 (at which time he became Chairman of University of California's Department 
of Biological Control). In addition to his responsibilities for planning and directing activities 
concerned with collecting, importing, and handling foreign insect natural enemies up to the time of 
their release to the appropriate Division for colonization and/or propagation, he continued other 
activities assigned to him including coordination of the work conducted by the other Divisions and 
cooperating states on the utilization of parasites and predators. For a short period during World War 
II, a Control Investigations Division was established, with Clausen serving also as its director. Thus, 
the foreign parasite introduction program was for this short period effectively under single 
management with control of both foreign and domestic work (Sailer 1981b). 


The two biological control laboratories in Europe were consolidated in 1935 when the Budapest 
laboratory (with W. F. Sellers in charge) was closed, and in 1936 the European Parasite Laboratory 
(EPL) was moved to St. Cloud near Paris. In 1939, this laboratory, which since 1922 had been 
headed by H. L. Parker, was closed due to the onset of World War II. During 1934-39, work at the 
EPL was conducted on natural enemies of the European corn borer, Hessian fly, European earwig, 
alfalfa weevil, asparagus beetle, pink bollworm, elm leaf beetle, European pine shoot moth, larch 
casebearer, pea weevil, and codling moth. Releases of European parasites of the larch casebearer in 
the 1930s made by both the USDA and Canada programs resulted in the establishment of two 
parasites (Agathis pumila and Chrysocharis laricinellae) which have provided substantial control of 
the pest in eastern U.S. and eastern Canada; with additional releases, this control was later expanded 
to western U.S. after spread of the pest there (see Appendix III below). (See references for the 


various EPL projects cited in Chapter I and especially Clausen 1956, 1978; Dowden 1962; and Drea 
1981.) 


Projects during 1934-41 at the Asian Parasite Laboratory (APL) in Japan, which was headed by R. 
W. Burrell from 1934 until closing of the laboratory in November 1941, included studies of the 
natural enemies of the oriental fruit moth, European corn borer, Comstock mealybug, Japanese 
beetle, Asiatic garden beetle, elm leaf beetle (for California), and European spruce sawfly (for 
Canada). Shipments of natural enemies of the first three pests were sent to Division of Fruit Insects’ 
laboratories at Moorestown, NJ, which also functioned as a quarantine receiving station. The oriental 
fruit moth project was another major USDA program entailing large scale rearing of the oriental 
parasites and their release in many Eastern states; only one of the parasites became established in the 
U.S. The Comstock mealybug program resulted in establishment of three parasites and commercial 
control of this pest was soon obtained in the eastern U.S. (See references for the various APL 
projects cited in Chapter I and Haeussler and Clancy 1944; Allen 1962; and Clausen 1956, 1978.) 


An European parasite of wheat stem sawflies obtained from the Canadian Department of Agriculture 
was released by USDA in the eastern U.S. in the 1930s. At first, no establishment was recorded 
(Clausen 1956), but much later the species (Collyria coxator) was found to be established, together 
with a second introduced parasite, in the eastern U.S., where complete control of the European wheat 
stem sawfly has been obtained (Streams and Coles 1965; Filipy et al. 1985). Other importations were 
made during the pre-war period of parasites of the sugarcane borer from Puerto Rico (where they had 
originally been established from Brazil) for Louisiana and Florida, and of the pink bollworm from 
Egypt, Korea, and Hawaii. (Clausen 1956, 1978.) 


In 1935-36, special funds were made available to USDA for a 1-year study of insect pests in Hawaii 
and Puerto Rico. Some of these funds were assigned to the Division of Foreign Parasite Introduction 
to conduct explorations for parasites of the Mediterranean fruit and melon flies for Hawaii, and 
importations of natural enemies of other insect pests for Puerto Rico. Fruit fly parasites were 
imported into Hawaii from four explorations (in West and East Africa, Brazil, India, and Sri Lanka) 
and from the Fruit Fly Laboratory in Mexico City, but there were no establishments, largely due to 
shipping problems and a precipitant cessation of funding (Clausen et al. 1965). A Division field 
station was established at Mayaguez, PR, under K. A. Bartlett, in cooperation with the federal 
experiment station there. Work concerned parasites of the sugarcane borer, West Indian fruit fly, 
coconut scale, pineapple mealybug, pink bollworm, limabean pod borer, white peach scale, and other 
pests. Parasite shipments were received from South American explorations, from Hawaii, the Mexico 
City laboratory, and mainland U.S. These Division efforts in Hawaii and Puerto Rico were concluded 
in late 1936. 


In 1937, a parasite quarantine receiving station was established within the Division of Foreign 
Parasite Introduction at the U.S. Entomological Laboratory at Moorestown, NJ. Laboratory facilities 
were constructed to enable foreign shipments to be received and handled under quarantine 
conditions, and for breeding of the parasites for shipments to other agencies throughout the U.S. This 
receiving facility, established at Moorestown in 1928, was to be the first of several such USDA 
biological control quarantine facilities. Personnel of the Moorestown Receiving Station were moved 
to new, improved quarters at the new Plant Quarantine Building at Hoboken, NJ, from 1940 until 
1944, when the Hoboken facility was closed (Clausen 1956). T. R. Gardner was in charge of the 
receiving facilities at Moorestown and Hoboken from 1937-43, when H. D. Smith was placed in 
charge. After closure of the Hoboken quarantine facility, shipments of imported natural enemies were 
received during 1945-52 at several Bureau of Entomology and Plant Quarantine field stations, the 
most important being the Division of Fruit Insects and Division of Cereal and Forage Insects 
laboratories at Moorestown, NJ, using the quarantine facilities there, and the newly opened Division 
of Foreign Parasite Introduction facility at Albany, CA (see below). 


16 


In 1938, additional studies were assigned to the Division of Foreign Parasite Introduction involving 
investigation of the effects of chemical and other control methods on populations of natural enemies. 
These studies were initiated at field stations in Orlando, FL (1938-40), Kearneysville, WV 
(1938-41), and Whittier, CA (1938-43). The major pests investigated included codling moth, 
strawberry leafroller, citrus whitefly, and several citrus scale insects. 


In 1938-39, a Division entomologist (P. A. Berry) conducted a survey of whitefringed beetles in 
South America, with little success in finding natural enemies. 


During World War II, the Division's Japanese and European laboratories were closed. The American 
personnel of the European Parasite Laboratory were sent to open a South American Parasite 
Laboratory in Montevideo, Uruguay, headed by H. L. Parker, which operated from January 1940 to 
November 1946. Explorations were conducted in various areas of South America, and temporary 
field stations were opened in Brazil and Peru. Over 300 shipments of natural enemies were sent from 
South America during this period. Most of the shipments were made to Hoboken, but some were 
made directly to other Bureau laboratories in Florida and Louisiana, and to the University of 
California. Major insect pests studied included Mexican bean beetle, pink bollworm, vegetable 
weevil, pea weevil, vetch bruchid, sugarcane borer, fall armyworm, corn earworm, and cotton 
leafworm. (Parker et al. 1950, 1953.) 


In 1936, a parasite of the asparagus beetle established in the eastern U.S. was collected in Ohio and 
established in Washington, which has resulted in partial, though not commercial, control of this pest 
in the latter state. Similarly, a cooperative University of California-USDA program in 1943 was 
successful in establishing in California an important parasite of the San Jose scale from the eastern 
U.S. This parasite has provided partial control of that pest in California. (Clausen 1956; DeBach 
1964). 


The citrus blackfly, which had been discovered in Mexico in 1935, spread rapidly throughout the 
citrus-growing areas of that country, and by 1950 was threatening citrus-growing areas of the U.S. In 
1938 and again in 1943, the Mexican Department of Agriculture, in cooperation with USDA's 
Division of Foreign Parasite Introduction, obtained and released the parasite that had successfully 
controlled this pest in Cuba; successful control was obtained only in areas of high humidity in 
Mexico. In 1943, a working agreement was negotiated by the governments of Mexico and the U.S. on 
biological, chemical, and quarantine measures to control this serious pest of citrus. In 1948-49, 
Division entomologists explored in Malaya, India, and Pakistan, and made many shipments of citrus 
blackfly parasites to the Division quarantine receiving laboratory at Mexico City, from which the 
parasites were disseminated and released in the principal citrus-infested areas of Mexico. This 
program resulted in the establishment of three Asian parasites and the subsequent complete economic 
control of the citrus blackfly in Mexico by 1953-55. This biological control success was to be 
repeated in Texas and Florida, when the citrus blackfly invaded those areas in the 1970s. (Smith and 
Maltby 1964; Thompson et al. 1986.) 


The discovery of the oriental fruit fly in Hawaii in 1946 resulted in funding for USDA foreign 
explorations and the establishment of another cooperative biological control importation program 
directed against this and other introduced fruit flies in Hawaii. In order to coordinate all phases of the 
project properly and prevent duplication of effort by the large number of participating agencies, a 
Memorandum of Agreement was established in 1948 involving USDA's Bureau of Entomology and 
Plant Quarantine, the Hawaiian Agricultural Experiment Station, the Hawaiian Sugar Planters' 
Experiment Station, the Pineapple Research Institute, and the University of California. Major 
responsibility for foreign exploration was assigned to the Bureau's Division of Foreign Parasite 
Introduction. During 1947-51, numerous shipments of over 25 species of parasites and predators 
were sent to Hawaii from the Philippines, Malaysia and other areas of Southeast Asia and Oceania, 


Ly 


southern China, Taiwan, India, Sri Lanka, and various areas of Africa, Brazil, Mexico, and Australia. 
During 1947-62, field releases were made of 29 species of parasites and one species of predator, and 
seven of the imported parasite species became established. Though full economic control was not 
attained, these and earlier established parasites are responsible for a considerable degree of 
parasitization and substantial reduction of fruit fly populations in Hawaii. (Clausen et al. 1965.) 


In 1944, the Division of Foreign Parasite Introduction established a laboratory at Albany, CA, headed 
by J. K. Holloway, in cooperation with the California Agricultural Experiment Station, to study the 
biological control of weeds (see below) and insect pests. And in January 1947, after the closing of 
the South American Parasite Laboratory, the Division's European Parasite Laboratory was reopened 
in France, under H. L. Parker. Projects initially assigned to the EPL included work on the European 
corn borer, sweetclover weevil, European chafer, and European elm scale, fig scale, and navel 
orangeworm in cooperation with the University of California. In 1950, projects on the European 
wheat stem sawfly, green peach aphid, omnivorous leaftier, and Rhodesgrass mealybug were added. 
Work on weeds had also begun there, in 1947 (see below). In June 1952, USDA explorations for 
natural enemies of the pink bollworm were begun in India, which resulted in the establishment of a 
USDA laboratory there that was maintained until 1958. G. W. Angalet was in charge of the Indian 
laboratory. 


In 1942, the Bureau of Entomology and Plant Quarantine was placed administratively under the 
Agricultural Research Administration of USDA. In April 1952, the Bureau's Division of Foreign 
Parasite Introduction was abolished and its personnel and functions combined with the Bureau's 
Division of Bee Culture to form the Division of Bee Culture and Biological Control, with its integral 
Biological Control Section absorbing the functions of the former Division of Foreign Parasite 
Introduction. Chief of the new Division was J. I. Hambleton, and T. R. Gardner was in charge of the 
Biological Control Section. (Gardner and R. Latta had been acting in charge of the Division of 
Foreign Parasite Introduction since Clausen's retirement in January 1951.) All parasite receiving 
activities at Moorestown, NJ, were placed under this new Division, and D. W. Jones, formerly with 
the Division of Cereal and Forage Insects, assumed leadership of the new Division's Foreign Parasite 
Introduction Station at Moorestown in July 1952. 


Significant accomplishments of the USDA's classical biological control program during 1934-1952 
included complete control of the citrus blackfly in Mexico (which was to be extended to Texas and 


Florida when that pest reached the U.S. in the 1970s) and of the European wheat stem sawfly and 
Comstock mealybug in the eastern U.S., substantial control of the larch casebearer in New England, 
and significant but partial population suppression of the San Jose scale, elm leaf beetle, and fig scale 
in California, and of the asparagus beetle in Washington State (Clausen 1956; Dowden 1962; 
DeBach 1964; DeBach and Rosen 1991; and Appendix III below). The two major USDA biological 
control importation programs, on the European corn borer and oriental fruit moth, had somewhat 
disappointing results. Six species of corn borer parasites were established in the U.S. and at first 
provided appreciable field control of this pest. However, the most effective of the introduced 
parasites, a tachinid fly, Lydella thompsoni, disappeared from the Corn Belt in the late 1950s, and 
corn borer populations rose. "At best it may be said that L. thompsoni bought the time needed to 
develop and place in production the borer-resistant hybrid varieties of corn" (Sailer 1973). Only one 
of the many oriental fruit moth parasites imported became established in the U.S., and it provides 
little control. However, the significant accomplishment in regard to the biological control program 
against this pest relates to augmentation (see below). 


The interest in biological control further declined during this period, with a continued shift toward 
insecticide research. The ratio of insecticide to biological control papers at the beginning of World 
War II was 6 to 1, and by 1946, 20 to 1, due to the development of DDT and many other synthetic 


_ insecticides. This trend is perhaps reflected in the organizational changes of 1952 noted above, i.e., 


18 


the abolishment of the Division of Foreign Parasite Introduction and its submersion into the Division 
of Bee Culture and Biological Control. However, by 1955 the trend had begun to reverse, the 
publication ratio then being 7 to 1. Despite these trends, the number of entomologists engaged in 
biological control research in the USDA increased up to the beginning of World War II to a high of 
about 40, and there was a subsequent decline during the 1940s, with a low of 5.5 scientific man-years 
(SYs) by 1954. During this period, more state organizations, in addition to those in California and 
Hawaii, became involved in the overall biological control program, wherein the USDA performed the 
initial exploration and importation phases and the states performed colonization and recovery phases. 
(Clausen 1956; Sailer 1973.) 


b. Augmentation and conservation of arthropod biological control agents. By J. R. Coulson 


Augmentation and conservation approaches during this period were focused on the oriental fruit 
moth program. A native species, Macrocentrus ancylivorus, a parasite of the strawberry leafroller, 
was found to attack the newly introduced pest moth, and attained a high degree of parasitization. 
Culture of this parasite and its release against the oriental fruit moth began as early as 1928, and the 
USDA mounted a large-scale release program in all infested areas of the eastern U.S. from 1929 to 
1935, during which 50% reduction of fruit injury was frequently reported. When the pest invaded 
California in 1942, Macrocentrus became the first parasite to be mass reared and released in an 
attempt to eradicate or prevent further spread of a pest. University of California researchers 
developed a low-cost, highly effective method for its mass culture, and millions were reared and 
released annually during 1944-46. Although overall eradication was unsuccessful, some infestations 
were eliminated. The parasite continues to be utilized in a number of state biological control 
programs to the present. However, in general, interest in the augmentation and conservation 
approaches to biological control, as well as in importation, waned as highly effective insecticides 
were discovered and came into general use. (Finney et al. 1947; Clausen 1956; Allen 1962; Sailer 
1973, 1976.) 


2. Arthropod-Parasitic Nematodes. By J. R. Coulson 


In 1934, the Bureau of Plant Industry was combined with other units and became the Bureau of Plant 
Industry, Soils, and Agricultural Engineering. The Division of Nematology continued under this 
Bureau, with its Chief, G. Steiner, 1932-56. Research on insect-parasitic nematodes continued at a 
few Division locations, though most of the research continued to emphasize plant nematodes. (See 
also Section C below on biological control of plant nematodes.) 


Considerable research was conducted during the 1930s on the biology and culture of the nematode 
Neoaplectana (now Steinernema) glaseri, discovered parasitizing the Japanese beetle in New Jersey, 
and a bacterium was discovered to be associated with it which caused the death of the Japanese 
beetle grubs. With the development of methods of mass culture of the nematode on artificial media, a 
large-scale colonization program was conducted in New Jersey in 1940 by the New Jersey 
Department of Agriculture in cooperation with the USDA and Rockefeller Institute for Medical 
Research at Princeton. A similar program was conducted later in Maryland. These first efforts to 
utilize nematodes for insect control did not produce effective control, and interest in the use of 
nematodes waned. Another nematode of this genus was discovered in 1954, which rekindled this 
interest; see Chapter III. (Fleming 1968.) 


3. Arthropod Pathogens. By J. R. Coulson, J. R. Adams, H. Shimanuki and P. V. Vail 
During this period, research on honey bee diseases, their control, and bee resistance to them, was 


conducted in the new Bureau of Entomology and Plant Quarantine created September 1, 1934, in the 
Bureau's Division of Bee Culture, under the leadership of J. I. Hambleton, 1924-52. This work was 


19 


primarily conducted at the Bee Culture unit at Beltsville, MD, and at the Laramie, WY, field station, 
by C. E. Burnside, E. C. Holst, A. P. Sturtevant and colleagues (Burnside 1934; Woodrow 1941a, 
1941b; Burnside and Revell 1948; Holst 1946; Burnside et al. 1949; Sturtevant 1949). For a brief 
period, 1952-1953, the Division of Bee Culture was combined with the Division of Foreign Parasite 
Introduction to form the Division of Bee Culture and Biological Control of the Agricultural Research 
Administration (see section A.1.a in this Chapter), with W. J. Nolan heading the Section of Bee 
Culture Research. (More information on USDA research on bee diseases is included in Appendix II.) 


At other Bureau of Entomology and Plant Quarantine locations throughout the U.S. administered by 
several Bureau Divisions, there were significant successes in utilizing pathogens for insect control. 
The first was the development by the USDA of the bacterial milky spore disease, Bacillus popilliae, 
found attacking the Japanese beetle in New Jersey (see Chapter I), into a highly effective, and 
economical control for that introduced pest. The Japanese beetle was discovered in New Jersey in 
1916, and soon became a severe, rapidly spreading economic pest, in part due to the absence of 
natural enemies. By the late 1930s, the USDA Japanese Beetle Laboratory at Moorestown, NJ, had 
expanded its staff to include R. T. White, I. M. Hawley, and S. R. Dutky. Research at the laboratory 
evolved into studies on most aspects of the use of the milky disease organism as a microbial control 
agent. Searches for diseased beetle grubs in New Jersey and studies of pathogens found were also 
conducted by Dutky and others. A bacterial microorganism was discovered, later described by Dutky 
as B. popilliae, that successfully controlled the grubs of this pest (Dutky 1940, 1941a-c, 1963; White 
and Dutky 1940). Methods for producing spores of the Bacillus and for storing and distributing them 
were developed. Procedures for mass production included injection of grubs with a microinjector, 
since the organism was not infectious per os (Dutky 1942a, 1947; Dutky and Fest 1942). Dutky then 
developed a spore dust formulation and application procedures for its effective use (Dutky 1942b). 
The spores were colonized in large areas of turf during 1939-53 in 14 states and the District of 
Columbia, providing effective suppression of Japanese beetle populations. Bacillus popilliae was 
further developed into the first commercial microbial pesticide, first officially registered for use in 
the U.S. in 1948. Dutky also studied other pathogens affecting the Japanese beetle, including the 
bacteria found in association with the nematode Steinernema glaseri, noted in the previous section. 
The Insect Pathology Unit of the Moorestown laboratory was moved to Beltsville, MD, in 1954 (see 
Chapter III). 


A second success in the utilization of insect pathogens for insect control was the development by the 
University of California of a nuclear polyhedrosis virus (NPV) as an effective control of the alfalfa 
caterpillar in California in the 1940s and early 1950s. Experiments with viruses were also conducted 
by Canadian researchers in the 1940s and 1950s for use against introduced forest insect pests. An 
exotic NPV virus was introduced into Canada from Sweden and utilized against the European pine 
sawfly in Ontario. Researchers from USDA's Division of Forest Insect Investigations conducted 
similar studies in the U.S. in 1951-52, with excellent results. The virus became widely used in both 
Canada and the U.S. (Bird et al. 1950; Dowden and Girth 1953; and Benjamin et al. 1955.) 


Toward the close of this period, research was being conducted on another insect bacterium, Bacillus 
thuringiensis, that led to the production of the most widely accepted, commercial microbial pesticide 
in use today. These successes increased interest in microbial control of insects, and insect pathology 
laboratories were established by the University of California in 1945, by the Canadian Department of 
Agriculture in 1946, and by the USDA in 1953. By the late 1950s and early 1960s, many other 
USDA laboratories began programs on insect pathology/microbial control. (Clausen 1956; Sweetman 
1958; Steinhaus 1964; Hall 1964; Heimpel 1974; Dutky 1991.) 


20 


B. BIOLOGICAL CONTROL OF WEEDS. By J. R. Coulson 


Following initiation of the use of insects for control of weeds in Hawaii, several other countries, 
including Australia, New Zealand, Fiji, India, and South Africa, became interested in this aspect of 
biological control in the 1920s and 1930s. The spectacularly successful control of the introduced 
prickly pear cactus in Australia by an insect introduced from South America kindled this interest 
even more. 


Biological control of weeds in North America began with joint USDA-University of California 
research on prickly pear cacti on Santa Cruz Island, California, in the late 1930s (Goeden et al. 1967; 
Goeden 1993). But it was not until 1944 that permission was granted for the introduction of exotic 
insects into the continental U.S. to control weeds. As noted above, USDA's Division of Foreign 
Parasite Introduction established a laboratory under J. K. Holloway at Albany, CA, that year for 
research on the biological control of weeds in cooperation with the University of California, and in 
1947, added research on natural enemies of introduced weeds to its European Parasite Laboratory in 
France. Initial target weeds for study at EPL included common St. John's-wort, from 1947, and gorse, 
from 1948. Common St. John's-wort, or Klamath weed, a rangeland weed, mildly poisonous to 
livestock, was introduced about 1900 into California, Oregon, and Washington, and by 1944 
occupied over two million acres of otherwise useful rangeland in California alone. The weed was 
also a pest in Australia, and European insects were studied and introduced into that country 
beginning in 1928; control of the weed was good in localized areas there. A similar program was 
authorized for the U.S., and importations of the European insects established in Australia were begun 
in October 1944, from Australia, importations from Europe being impossible due to the war. Two 
species of beetles became established almost immediately, and by 1947 no further importations of 
those beetles were needed. In 1950, millions of the beetles were collected in California for 
recolonization. 


At the close of the war, research on other European enemies of common St. John's-wort/Klamath 
weed was begun at the reopened European Parasite Laboratory in 1947, and shipments were made to 
California. By 1954, populations of the weed in California were reduced to the level of a roadside 
weed, and is now estimated to occupy less than 1% of its former abundance. The replacement 
vegetation was comprised primarily of native plants. Grateful California ranchers erected a 
monument in Fortuna, Humboldt County, to the beetles responsible for this control, the benefits of 
which are estimated at $23,000,000 per year over previous control costs plus weight gain in cattle. 
Much of these benefits extended to Oregon, Washington, Idaho, and other western states. (Holloway 
1964; Huffaker and Kennett 1959; Huffaker et al. 1976; Goeden 1978.) 


C. BIOLOGICAL CONTROL OF PLANT NEMATODES. By R. M. Sayre 


As noted in the above section on insect-parasitic nematodes, the USDA Division of Nematology 
Investigations continued, under the leadership of G. Steiner (1932-56), within the newly reorganized 
Bureau of Plant Industry, Soils, and Agricultural Engineering, formed in 1934. This Bureau was 
placed administratively under USDA's Agricultural Research Administration in 1942. 


In 1935, C. Drechsler, a USDA plant pathologist, was relocated from downtown Washington, DC, to 
the newly opened research facility at Beltsville, MD. There, he continued studies on the numerous 
soil fungi parasitizing amoebae, tardigrades, testaceous rhizopods, and nematodes. Drechsler was not 
a nematologist, but a mycologist in the Bureau's Horticultural Crops Research Division. His work 
was of direct benefit to the science of nematology. At retirement in 1962, he had published over 180 
papers, some sixty of which included descriptions of new species of nematode-destroying fungi. 
These publications, even today, serve as guides to others in their search for fungi that might be used 
as biological control agents of nematodes. Although he suggested that fungi were regulators of 


a1 


nematode populations, he never determined which fungal species might best be used in a practicable 
method for control of nematodes in agricultural soils. 


During this period, there was one landmark field plot study, that of M. B. Linford and others of the 
Pineapple Experiment Station, University of Hawaii (Linford 1938). In field plots, they found 
reductions of soil populations of root-knot nematodes during the decomposition of organic matter 
that had been added to the soils. They attributed this reduction of nematodes to the fact that organic 
matter may have stimulated the activities of the many soil antagonists of nematodes. This was, 
perhaps, one of the first field tests that demonstrated biological control of nematodes. 


In 1940, G. Thorne published on the life cycle of a "protozoan" parasite of a Pratylenchus nematode 
species (Thorne 1940). Again, as in his 1927 paper (Thorne, 1927), he pointed out the potential of 
this organism as a biological control agent. 


In the same year (1935) that Drechsler moved to Beltsville, A. L. Taylor established a USDA field 
station at Tifton, GA. Later, Taylor served as a technologist for Shell Oil Company, 1946-49, where 
he did pioneering work towards the development of a volatile nematicide suitable for injection into 
soils. His work helped lead the way to the discovery and development of volatile D-D 
(1,3-dichloropropene and 1,2-dichloropropane) mixtures, EDB (1,2-dibromoethane), and DBCP 
(1,2-dibromo-3-chloropropane) in 1943, 1945, and 1954, respectively. (Christie, the USDA 
nematologist, determined the efficacy of EDB [Christie 1945].) These nematicides were to 
profoundly change the management practices used to control plant-parasitic nematodes. Attention 
was diverted from previously used methods to a single chemical tactic. This control approach 
dominated the thinking and actions of most nematologists for the next two decades. 


D. BIOLOGICAL CONTROL OF PLANT PATHOGENS. By R. J. Cook, G. C. Papavizas, and 
J. R. Coulson 


Considerable research on plant pathogens and their control was conducted during this period by 
many plant pathologists in various units of USDA's Bureau of Plant Industry, Soils, and Agricultural 
Engineering (Stefferud 1953). However, though some research on biological control of plant 
pathogens was conducted elsewhere (Wood and Tveit 1955), there was little study in this area within 
the USDA during this period. 


Hurley Fellows and C. H. Ficke, both of USDA's Bureau of Plant Industry, Cereal and Forage Crop 
Disease Investigations, at Manhattan, KS, worked on root diseases of wheat. Their pioneering studies 
on take-all caused by Gaeumannomyces graminis var. tritici included significant observations on 
biological control (Fellows and Ficke 1934). Workers in Canada and Texas had shown earlier that 
root rots could be controlled by intensifying the activity of soil saprophytes by use of green or 
barnyard manure. Fellows and Ficke demonstrated this same effect for wheat take-all using various 
sources of organic materials, including chicken manure. Studies by F. E. Clark, of USDA's Bureau of 
Plant Industry, Soil and Fertilizer Investigations, showed that the suppressive effect of organic 
amendments on take-all and Phymatotrichum root rot was the result of intensified antagonism of the 
causal pathogens by microorganisms stimulated by the added substrates (Clark 1942). Fellows and 
Ficke (1934) had reported that take-all disappeared after about the fourth year of continuous wheat, 
and severe disease in the second and third years of wheat monoculture, an observation that would 
prove to be one of the first reports of biological control being responsible for "take-all decline." 
However, proof that take-all decline results from spontaneous biological control would not emerge 
until the 1960s (see below). 


Bis 


CHAPTER III 
1953-1972 
AGRICULTURAL RESEARCH SERVICE 


A. BIOLOGICAL CONTROL OF ARTHROPODS (INSECTS, MITES, AND TICKS) 
1. Arthropod Biological Control Agents 


a. Classical biological control (introduction of biological control agents). By J. R. Coulson and 
W. H. Day 


In November 1953, the old Agricultural Research Administration became the Agricultural Research 
Service (ARS), and the Bureau of Entomology and Plant Quarantine was abolished, its regulatory 
functions being placed into the Plant Quarantine and Plant Pest Control Branches (later Divisions) 
under ARS, and its research functions being placed in the newly formed Entomology Research 
Branch (raised to Division in 1957). Forest entomology was removed from ARS and placed in 
USDA's Forest Service (see notes on subsequent biological control activities in the Forest Service in 
Chapter V), and research on stored-products insects was assigned temporarily to the Agricultural 
Marketing Service, but later was returned to ARS. E. F. Knipling was designated Chief (Director in 
1957) of the new Entomology Research Branch/Division and remained in charge until 1971. C. H. 
Hoffmann and H C Cox served as Division Directors from January 1971 until June 30, 1972, when 
the Division was abolished, and after 91 years (1881-1972), entomology ceased to be a separate 
entity within the USDA. (Rainwater and Parencia 1981.) 


At the start of this period, there was an increasing awareness of problems caused by emphasis on 
chemical control of pests: development of insect resistance to chemical pesticides; concern over 
pesticide residues; and new pests developing due to destruction of their natural enemies by 
broad-spectrum pesticides. A 1953 review of the entomological research program indicated the need 
to make a substantial shift from chemical control to biological control, and this was immediately 
implemented by the Entomology Research Branch/Division, which increased research on alternative 
methods of pest control, and strengthened research on parasites, predators, and pathogens. This was 
reflected in an increase in the number of man-years devoted to biological control of insect crop pests 
from 5 in 1954 to 52 by 1965, and in the number of man-years devoted to biological control of weeds 
from 0.5 in 1954 to 6 in 1965. But due to general curtailment of government expenditures, the total 
number fell to 43 by 1972 (Sailer 1973). 


On July 1, 1954, the Biological Control Section was removed from the old Division of Bee Culture 
and Biological Control and combined with the Insect Identification Section of the old Division of 
Insect Detection and Identification to form the new Insect Identification and Parasite Introduction 
(IIPI) Research Section (or Laboratory), which was raised to Branch status in 1957. Chiefs of this 
Section/Branch were P. W. Oman, 1954-60, W. H. Anderson, 1960-67, and R. I. Sailer, 1967-72. The 
IIPI was abolished with the Entomology Research Division on June 30, 1972. This reorganization 
effectively ended, after 38 years (1934-72), the centralized leadership and coordination of USDA's 


23 


foreign and domestic classical biological control importation programs that proved so successful for 
biological control. 


The IIPI was given responsibility for conducting research in foreign areas, and for directing work at, 
and maintaining, all USDA biological control quarantine receiving stations in the U.S. Other 
commodity-oriented Sections/Branches of the Division were responsible for all aspects of parasite 
and predator studies that concerned pests within the scope of their commodity responsibilities. These 
included work with exotic species from the time natural enemies were cleared from quarantine and 
research on the effects of pesticides on the insects and their natural enemies. These types of research 
were conducted in close coordination and cooperation with IIPI. The combination of 
parasite/predator research with insect systematics was intended to facilitate maximum identification 
service for biological control, and to permit the use of USDA taxonomists in initial biological control 
surveys, collections, and field identifications. 


At the time of the 1953-54 reorganization, three foreign laboratories reported to IIPI: Mexico City, 
Mexico (1953-57) (H. D. Smith in charge), New Delhi, India (1953-58) (G. W. Angalet in charge), 
and the European Parasite Laboratory (EPL) near Paris, France (1953-72) (directed by H. L. Parker, 
1953-60; R. I. Sailer, 1960-65; R. J. Dysart, 1965-69; J. J. Drea, 1969-80). Each laboratory was 
staffed by a single American entomologist, and the Indian and European laboratories had additional 
local staff. A second American was added to the EPL in the early 1960s. Other IIPI foreign locations 
were established later during this period for studies on the biological control of weeds (see section B 
below). 


Work at the Mexico City laboratory was essentially the continuation of the citrus blackfly project 
discussed in Chapter II, cooperation in various aspects of biological control with the Mexican 
Department of Agriculture, and studies of natural enemies of citrus pests in the Rio Grande Valley of 
Texas. Work at this location was terminated at the end of 1957. 


Major work at the New Delhi laboratory concerned natural enemies of the pink bollworm (1952-54) 
and spotted alfalfa aphid (1955-58). Miscellaneous observations and opportunistic collections of 
natural enemies of other U.S. pests were made in India, including, but not limited to, bollworm, 
epilachnine beetles, citrus whitefly, California red scale, Rhodesgrass mealybug, pea aphid, and the 
weed puncturevine. This laboratory was closed in 1958. } 


Studies at the European Parasite Laboratory concerned natural enemies of several weeds (see Section 
B below) and a number of insect pests including the following: sweetclover weevil, for North Dakota 
(1953-62); wheat stem sawfly, for North Dakota, Nebraska, and Montana (1953-55); Rhodesgrass 
mealybug, for Texas (1953-59); European chafer, for New York (1953-60); green peach aphid, for 
western and eastern states (1953-58); omnivorous leaftier, for the Pacific Northwest (1954-55); 
cherry and apple maggots (1954-64); yellow clover aphid (1955-56); vetch bruchid (1955-65); 
spotted alfalfa aphid (1955-56); alfalfa weevil (1959-72); alfalfa and clover seed chalcids (1959-64); 
pea aphid (1959-69); balsam woolly adelgid (1959-64); European pine shoot moth (1961-65); face 
fly (1961-67); lygus bugs (1962-65 and 1970-72+); cereal leaf beetle (1963-73); grasshoppers 
(1963-71); smaller European elm bark beetle (1963-68); imported cabbageworm (1967-69); greenbug 
(1968-71); "linden aphid" (Eucallipterus tiliae), for California (1969-70); alfalfa snout beetle, for 
New York (1970-72); elm leaf beetle, for California (1971-73); and gypsy moth (1972+). 


Two domestic field locations also reported to IIPI in 1953 - an East Coast Parasite Receiving Station 
located at Moorestown, NJ (1953-73) (headed by D. W. Jones, 1953-60; L. B. Parker, 1961-63; 

M. H. Brunson, 1963-70; L. W. Coles, 1970-71; W. H. Day, 1971-78), and West Coast Parasite 
Receiving Stations located at Albany, CA (1953-57) (J. K. Holloway in charge), and Riverside, CA 
(1957-68) (headed by B. Puttler, 1957-59, and D. W. Clancy, 1961-68), and operated in cooperation 


24 


with the California Agricultural Experiment Stations at Albany and Riverside, respectively. The New 
Jersey station received most of the parasite/predator shipments from the Indian and European 
stations. The California station at Albany was responsible mostly for receipt of shipments of natural 
enemies of weeds (see section B), but also received parasite/predator shipments from the European 
station that were destined for use in western states, and from University of California explorers (e.g., 
a number of shipments of beet leafhopper parasite material from Morocco and Egypt was received at 
the Albany station from 1953-54). The Receiving Stations were responsible for clearing foreign 
material through quarantine to assure that only beneficial species were released from quarantine, and 
for distribution of the material to State and federal researchers and action agencies for study and field 
release. Personnel at both the East Coast and West Coast stations also participated in research 
programs involving release and evaluation of exotic natural enemies in their respective areas. 
Projects at the Riverside location included spotted alfalfa aphid, alfalfa weevil (for the East Coast), 
Egyptian alfalfa weevil, elm leaf beetle, limabean pod borer, pea aphid, lygus bugs, cabbage looper, 
Comstock mealybug, and vegetable weevil. In the early years, the New Jersey station was mainly 
involved only in quarantine clearance, culture, and distribution of the imported natural enemies 
received. However, in 1956, breeding of aphid parasites and predators for release in New Jersey was 
begun, and some sweetclover weevil parasites were released in New Jersey and Delaware beginning 
in 1957. Other more extensive release and field evaluation projects soon developed at the 
Moorestown location, including those on wheat stem sawfly (1957-64), pea aphid and other aphids 
(1958-72+), alfalfa weevil (1958-72+), apple, cherry and blueberry maggots (1959-62), lygus bugs 
(1962-72+), face fly (1966-69), Mexican bean beetle (1967-68), and alfalfa blotch leafminer 
(1971-72+). The station's major project on alfalfa weevil biological control was an outstanding 
success (see below). 


In 1965, a third domestic location was added to IIPI, a newly constructed Biological Control of 
Insects Research Laboratory at Columbia, MO. Directors of this Laboratory were F. R. Lawson 
(1965-70) and C. M. Ignoffo (1971-1989). The purpose of the Laboratory was to develop and test 
new principles and methods of using parasites, predators, and pathogens against major insect pests, 
with emphasis on reduction of pest populations over large areas by integration of biological control 
measures with other control measures such as pesticides, sterile insect techniques, attractants, 
cultural methods, etc. Initial projects at the Laboratory included biological control of 1) insect pests 
of cole crops, 2) insect pests attacking leaves and stems of crop plants, 3) insects attacking roots of 
plants, and 4) flies attacking man and animals. These included research on host and parasite rearing 
(including Trichogramma egg parasites), field observations and experiments (primarily with cabbage 
insects and cutworms), and work on integrated control of livestock insects (primarily horn fly). In 
this period, research at this Laboratory demonstrated successful control of cabbage insect pests by 
use of parasites and pathogens (Parker et al. 1971; see Augmentation section below). 


During this period, IIPI and other Entomology Research Division Branches followed the custom 
begun in the Bureau of Entomology and Plant Quarantine era of requiring all foreign and domestic 
locations to submit quarterly reports of their activities. These reports have been important sources of 
information when projects have been reopened after a period of years, or when new personnel 
became involved in an old project. They have been of special importance for foreign explorations, 
and in the preparation of this history. 


In 1958, the Foreign Agricultural Research Grant Program was initiated under authority of U.S. 
Public Law 480 (the Agricultural Trade, Development, and Assistance Act of 1954). This program 
continues today as the Special Foreign Currency (SFC) program. P.L. 480 authorizes USDA to use 
U.S.-owned foreign currencies to support cooperative agricultural and forestry research on problems 
of interest to the U.S. and participating foreign countries. This program, which until 1978 was 
administered by ARS, has been of special importance to USDA's biological control programs, and its 
taxonomy programs. From 1959-72, IIPI scientists were "cooperating, or sponsoring, scientists" on 


oe) 


numerous biological control and taxonomic projects in Brazil, Colombia, Uruguay, Egypt, Morocco, 
India, Pakistan, Taiwan, Korea, Israel, Yugoslavia, and Poland. The biological control projects 
generally concerned surveys for natural enemies of certain crop pests, or in certain crop or ecological 
situations, and represented a considerable expansion of USDA's biological control exploration 
program. Extensive valuable information was accumulated concerning the natural enemies of insect 
and weed pests in these areas, much of which remains in unpublished reports, which are on file in the 
ARS Biological Control Documentation Center. Later projects concerned research on techniques for 
culturing or otherwise utilizing specific types of natural enemies. Taxonomic projects under the P.L. 
480 program contributed important information on the systematics of parasitic and predaceous 
groups, including descriptions of new species of importance to biological control. Many of the 
natural enemies discovered or described during these various projects were imported for study and 
release against insect and weed pests in the U.S. Projects in the U.S. which benefitted included those 
concerning the balsam woolly adelgid, cereal leaf beetle, gypsy moth, corn earworm/ 
bollworm/tomato fruitworm, various aphids and scale insects, European corn borer, sugarcane borer 
and other stalk borers, Trichogramma egg parasites, beneficial and non-beneficial lady beetles, plant 
bugs, dung beetles, fruit flies, and leafminer flies, among others. 


In addition to these overseas activities, personnel of ARS' Plant Protection Division (PPD) (now the 
Plant Protection and Quarantine Programs of the Animal and Plant Health Inspection Service) were 
involved, from 1967-69, in shipment of large quantities of several gypsy moth parasites from Spain. 
These parasites were collected in connection with PPD's studies on sex attractants there, and PPD 
financed collections of gypsy moth parasites in Yugoslavia in 1970. These parasites were cleared in 
ARS quarantine at Moorestown, NJ, and made available for release by PPD and state personnel in 
several northeastern states, especially NJ and PA (Reardon and Coulson 1981). 


Significant accomplishments resulting from ARS's biological control importation program during 


1953-72 included, but are not limited to, the control of three serious introduced pests, the cereal leaf 
beetle and the alfalfa weevil in the eastern U.S., and the Rhodesgrass mealybug in Texas. 


The cereal leaf beetle (CLB), a European species, was discovered to be established in Michigan in 
1962, and was quickly recognized as a major threat to U.S. small grain production. ARS studies at 
the European Parasite Laboratory began in 1963 and resulted in the discovery and importation of five 
species of parasites of the beetle through ARS quarantine. Since there were no IIPI units within 
working distance of the pest populations, release and establishment work was conducted first under 
cooperative agreements with universities in Michigan and Indiana. In 1966, the Plant Protection 
Division of ARS (which in 1971 became the Plant Protection and Quarantine Program (PPQ) of 
USDA's new regulatory agency, the Animal and Plant Health Inspection Service [APHIS]), 
established a laboratory in Michigan to culture and/or otherwise disseminate and release the 
introduced parasites. By 1972, four of the European parasite species were established in the U.S., and 
through the efforts of PPQ were soon disseminated and established throughout the expanded range of 
the CLB, which soon covered most of the northeastern U.S. and some parts of eastern Canada. 
Though the absence of research involvement in much of the domestic phase of this program long 
prevented a thorough, detailed evaluation of its results, the program is recognized as an outstanding 
success, the parasites being credited with economic control of this pest. Heavy crop losses (as high as 
55% in spring grains and 23% in winter grains; R. J. Dysart, personal communication, 1984) reported 
during the late 1960s in the Midwest were nearly eliminated, and this pest seldom reached damaging 
levels as it later expanded its range. An assessment of the benefits of this program made in 1978 by 
the APHIS laboratory in Niles, MI (W. H. Day, unpublished data, 1988; see Table 1) noted a 
conservatively estimated annual savings of $14,000,000 due to cessation of many pesticide 
applications previously applied for this pest; e.g., 1.6 million acres were treated in 1966, but only 
20,000 acres in 1981 (R. J. Dysart, personal communication, 1984). Incidentally, this was the first 
example in which a pest of an annual crop in a temperate continental area was successfully controlled 


26 


by imported parasites. Previous successes had been with pests of perennial crops. (Dysart et al. 1973; 
Sailer 1973, 1981a; Coulson 1976; Burger 1980; Haynes and Gage 1981; Lampert and Haynes 1985; 
DeBach and Rosen 1991.) See also Chapter VI for more complete information on the APHIS 
program, including updated cost:benefit information. 


In 1951, the alfalfa weevil, which had been present in the western U.S. since the early 1900s, was 
found in Maryland and by 1971 had spread throughout most of the eastern U.S. It became the number 
one pest of alfalfa in the East, requiring regular insecticidal treatments to prevent total crop 
destruction in most cases, and in some cases, especially in the Southeast, farmers were forced to shift 
from alfalfa production to less desirable forage crops. The discovery of insecticide residues in milk, a 
result of cows eating alfalfa contaminated with the hazardous pesticides in use at the time, was an 
additional serious problem. IIPI scientists at the European Parasite Laboratory and the New Jersey 
parasite receiving facility began a parasite importation program in 1957. The weevil parasite 
established earlier in the West, was successfully recolonized by ARS in New Jersey by 1959 and 
quickly spread throughout the East. However, it soon became clear that one parasite species would 
not provide adequate biological control of this pest. By 1965, five parasite species were established 
in the New Jersey-eastern Pennsylvania area and began to disperse throughout the Middle Atlantic 
States. (A total of seven species were eventually established; Dysart and Day 1976; Dysart 1989; 
Bryan et al. 1993.) The New Jersey Department of Agriculture developed a strong parasite 
distribution program, aided by the ARS Moorestown station, that resulted in rapid expansion of 
parasite populations in that state. By 1970, weevil populations there had decreased and only 8% of 
New Jersey farmers used insecticides for the weevil, as compared to 94% in 1966, saving farmers 
$3,000,000 in 1970 in this state alone. ARS Moorestown personnel also collected and disseminated 
the parasites to other states from 1965-72, and the parasites continued to increase and spread. By 
1978-79, their effects on the weevil were significant, saving farmers in an 11 state area in the 
Northeast about $8,000,000 annually due to cessation of previously applied insecticidal treatments. A 
more recent estimate (W. H. Day, unpublished data, 1988; see Tables 1 and 2) of such savings to 
farmers in 18 eastern states as the parasites’ ranges have increased further is, by 1986, nearly $49 
million annually. Adjusted for inflation to 1993, this annual savings represents $63,700,000! This is 
a considerable return for an estimated total cost of about $1,000,000 for the ARS importation 
program. The dissemination of the parasites by ARS personnel was recognized as detracting from the 
ARS research programs, and this work was assumed by APHIS in 1980. Improvements in this aspect 
of biological control, i.e., implementation, are discussed in subsequent chapters. (Sailer 1973, 198 1a; 
U.S. House of Representatives 1973; Coulson 1976; Day 1981; Lashomb et al. 1988; Moffitt et al. 
[1990]; Bryan et al. 1993.) 


The Rhodesgrass mealybug, an oriental species, was first identified in the U.S. in 1942 and quickly 
became a major pest of forage and lawn grasses in Texas in the 1940s. A parasite of the mealybug 
known from Hawaii was imported and established in 1949 and was reared and released in large 
numbers by the Texas Agricultural Experiment Station (TAES) in cooperation with the USDA. 
Mealybug parasites were also sent to Texas from USDA's European Parasite Laboratory in the 1950s. 
These attempts provided little control of the mealybug. In 1956, the ARS entomologist at the Indian 
station discovered an undescribed parasite attacking the mealybug, now known as Neodusmetia 
sangwani (Subba Rao). This species was introduced into Texas in 1959 where it became established 
and control of the mealybug was quickly demonstrated. Methods were developed by the TAES to 
distribute the parasite throughout Texas rangelands in the 1960s, and the Rhodesgrass mealybug was 
eliminated as a pest of forage grasses in Texas by 1970. A 1979 cost:benefit analysis indicates that 
this successful control represents an annual savings of almost $17,000,000 in reduced costs for turf 
grass maintenance alone, and additional profits from increased calf sales exceeding $177,000,000. 
Total cost of the project in Texas was less than $200,000. The parasites have also been established in 
Florida with nearly similar results. (Sailer 1973; Dean et al. 1979; DeBach and Rosen 1991.) 


2] 


In addition to these three successful classical biological control programs, other accomplishments 
during 1953-72 included the establishment of parasites and predators of a number of other introduced 
insect pests in the United States, of which the most noteworthy are the spotted alfalfa aphid and the 
pea aphid. The spotted alfalfa aphid appeared in California in 1954 and quickly spread across the 
southern U.S., inflicting severe damage to alfalfa crops. The USDA and University of California 
began a cooperative biological control program in 1955 that resulted in establishment of three 
parasites and their rapid dispersal across the range of the aphid. In the meantime, straihs of alfalfa 
were being developed that were resistant to the aphid. By 1958, spotted alfalfa aphid outbreaks had 
subsided due to a combination of plant resistance and parasitism, and aphid populations remain 
below economic levels today. The pea aphid was a much earlier introduction, being found in North 
America in the 1870s (Davis 1915), and by the 1950s was distributed throughout the continental U.S. 
as a very important pest of peas, alfalfa, and other leguminous crops. In the late 1950s, parasites were 
introduced by ARS from India and Europe, established, and quickly dispersed throughout the U.S. 
After the mid-1960s, there was a marked reduction in reports of damage caused by the pea aphid. It 
has been estimated that an annual savings of over $36,000,000 has resulted from a 30% reduction in 
alfalfa acreage no longer treated for this pest (W. H. Day, ARS, unpublished data, 1988); adjusted for 
inflation, the savings represent $47,300,000 in 1993 dollars (see Table 1). A third introduction of 
note was that of the staphylinid face fly predator, Aleochara tristis, which was the first natural enemy 
of livestock pests introduced by ARS. This species was imported in 1965, cultured in Nebraska, and 
released in several western and eastern states. It became established in Nebraska, but has had little 
apparent impact on the pest to date. (van den Bosch et al. 1959; DeBach 1964; Drea 1966; Sailer 
1973; U.S. House of Representatives 1973; Angalet and Fuester 1977.) 


Thus, the results of USDA's classical biological control program during this period have produced a 
total, conservatively estimated benefit of at least $115,000,000 a year, or $150,000,000 in 1993 
dollars, benefits that accrue annually! These savings figures compare very well with the estimated 
total costs ($20,000,000) of research by both Federal and State agencies to find, establish, and utilize 
natural enemies of insect and weed pests from 1888 to 1976 (Sailer 1976), and with the estimated 
$420,000,000 spent annually on insecticides in the 1960s (Sailer 1973). 


It was during this period that Rachel Carson published Silent Spring (1962), which increased public 
concern about the effects of pesticides in the environment, which in turn led to an increased interest 
in biological control and other nonchemical methods of pest control. In regard to classical biological 
control, USDA's Insect Identification and Parasite Introduction Research Branch (IIPI) gradually 
broadened the scope of its activities to include not only foreign exploration and importation 
activities, but also domestic release and evaluation activities on pests located within working 
distances of its domestic research locations. Thus in effect, there was single, close administrative 
coordination of the alfalfa weevil parasite importation program from its foreign exploration and 
quarantine receiving aspects, to its release and evaluation (establishment and effectiveness) phases, 
and resources (funds, personnel, etc.) could be readily shifted from one area to another as dictated by 
program needs. This is seen by many to be an ideal situation for optimal conduct of parasite 
introduction programs, and seems to have paid off in the case of the alfalfa weevil program. There 
was, however, a need for a better method of dissemination of effective, established parasites, in the 
case of the alfalfa weevil program, to include non-research input. This goal was accomplished at the 
state level, very effectively by the New Jersey Department of Agriculture, but was not addressed 


until later at the federal level, in the period after 1972. (Sailer 1974, 1976b, 1981b; Coulson 1976; 
Lashomb et al. 1988.) 


28 


b. Augmentation and conservation of parasites and predators. By D. A. Nordlund, E. G. King, C. J. 
DeLoach, and P. V. Vail 


During this period, Rachel Carson (1962) published Silent Spring. Though the problems cited by 
Carson were recognized by many in the scientific community, her book attracted the attention of the 
general public. The resulting public outcry against the indiscriminate use of conventional pesticides 
resulted in a considerable increase in research to develop alternative pest management techniques. 
Evidence of pests developing resistance to pesticides and of the harmful effects of pesticides on 
non-target organisms also increased. Several relatively new approaches to the control of insect pests, 
including the use of pheromones and hormones, came into the limelight. Integrated pest management 
(IPM), which is, to a great extent, a conservation approach, also began to take on an increased role in 
pest management. Biological control also received attention and there was increasing awareness on 
the part of biological control workers that not all of the insect pest problems in the U. S. were 
amenable to the classical importation approach. Many of the pests are native and have a full 
complement of natural enemies already attacking them. Researchers also began to realize that the 
annual row crop agroecosystem is, because of the disruptions that occur in such systems, a difficult 
place for natural enemies to work without man's assistance. Thus, augmentation and conservation 
began to receive increased attention, at least during the latter part of this period. 


Much of the biological control work conducted by ARS scientists during this period was basic 
biological and ecological studies of parasites and predators that could possibly be used in 
augmentation or conservation programs. Though a number of pests were involved in the research that 
is discussed here chronologically, the major targets of such research during this period included 
lepidopterous and hemipterous pests in cotton, lepidopterous pests in cabbage, and scale insect pests 
in citrus. Research on the use of Jrichogramma continued in ARS and elsewhere in the U.S., but 
utilization of these biological control agents was most intensive in other countries, such as the USSR, 
China, and Mexico. 


Lawson (1959) studied natural enemies of the tobacco and tomato hornworms and found that egg and 
larval predators, especially Polistes wasps, and Cotesia (=Apanteles s. lat.) parasites caused 
significant pest mortality. DeLoach and Rabb (1971, 1972) found that the tachinid, Winthemia 
manducae, caused significant losses of hornworm prepupae. These natural enemies often maintained 
complete control of the pests and significantly reduced crop losses. Finney et al. (1960), of the 
University of California at Berkeley, in cooperation with ARS's Ben Puttler, developed rearing 
techniques for three hymenopterous parasites of the spotted alfalfa aphid. These techniques were 
developed to facilitate an augmentation program against this pest. Puttler (1961) studied the biology 
of Hyposoter exiguae, a parasite of lepidopterous larvae. Wene and Sheets (1962) studied the role of 
predatory insects in the Salt River Valley (Arizona) area cotton and found that the naturally 
occurring predators could not maintain control of lygus bugs (Lygus spp.), whitemarked fleahopper 
and western plant bug, and cotton leafperforator (or the saltmarsh caterpillar). Also in 1962, Burrell 
and McCormick reported that releases of Trichogramma against the sugarcane borer resulted in no 
significant increase in parasitism of borer eggs. 


In 1962, under the leadership of Orin Hills, a biological control program was initiated at the Western 
Vegetable and Sugarbeet Investigations, Mesa, AZ. Initially, the objective was to catalog the 
parasites of noctuids attacking vegetable and row crops in the desert areas of the southwestern U.S. 
R. W. Brubaker assumed responsibility for, and expanded this program to include surveys of the 
relative abundance of several parasites of noctuids, with particular emphasis on tachinids (Brubaker 
1968). Following these surveys, three species were selected for further study, in support of 
augmentative releases to control the cabbage looper and the beet armyworm on an area wide basis. 
These studies led to the integration of the use of parasites with other methods, such as 
pheromone-baited light traps and sterile insect techniques then being developed at the laboratory. 


29 


The parasites initially selected were Lespesia archipivora, a tachinid parasite of the beet armyworm, 
and two parasites of the cabbage looper: Copidosoma truncatellum, a polyembryonic egg-larval 
hymenopteran; and Voria ruralis, a tachinid. Rearing of these parasites was facilitated by 
development of semi-artificial diets for their hosts (Henneberry and Kishaba 1966; Shorey and Hale 
1965; van der Zant 1966). Various biological, behavioral, and efficacy studies were also conducted 
with these parasites (Brubaker 1968). Brubaker, who retired in 1970, was replaced by C. Soo Hoo. 
Field cage and behavioral studies were subsequently conducted with the two tachinids (Soo Hoo et 
al. 1974), which demonstrated that V. ruralis could provide high levels of parasitism. 


Biological control related research began increasing significantly about 1966. That year, Dolphin and 
Cleveland (1966) reported their studies of Trichogramma minutum as a parasite for use against the 
codling moth and redbanded leafroller. The behavior of Campoletis flavicincta (as perdistinctus), a 
parasite of the tobacco budworm, was studied by Noble and Graham (1966). Knipling (1966) 
developed theoretical predator/prey ratios required to obtain various levels of control in periodic 
release programs. Kieckhefer and Miller (1967) studied aphids and aphid predators in South Dakota 
cereal crops and found that aphid population increases in cereal crops were primarily dependent on 
movement from other crops. Hendricks (1967) studied effects of wind on dispersal of Trichogramma 
semifumatum and worked on release technology for this egg parasite. Burrell (1967) studied parasites 
that attack the armyworm. Champlain and Sholdt (1967a,b) studied the basic biology of the generalist 
predator Geocoris punctipes. Streams and Fuester (1967) studied Oomyzus (=Tetrastichus s. lat.) 
incertus, an imported parasite of the alfalfa weevil, while Hagen and Manglitz (1967) studied 
parasitism of the alfalfa weevil in the western plain states. Puttler (1967) found that encapsulation of 
Bathyplectes curculionis eggs by the weevil was common in the eastern U.S., but not in the western 
U.S. Lingren et al. (1968) studied consumption of Heliothis (s. lat.) spp. eggs and larvae by several 
common arthropod predators. Puttler and Dickerson (1968) studied the biology of Apanteles forbesi, 
a parasite of the bristly cutworm. Clancy (1968) studied the distribution and parasitization of Lygus 


spp. 


In 1969, Marston and Ertle reported on some basic studies of parasitization by Trichogramma 
minutum, while Lewis and Redlinger (1969) tested the eggs of almond moth as hosts for 
Trichogramma evanescens. Ridgway and Jones (1969) reported on inundative releases of the 
common green lacewing for control of Heliothis (s. lat.) spp. on cotton. Adams et al. (1969) reported 
on the biology of Bracon mellitor, a parasite of the boll weevil and suggested that inundative releases 
of this parasite could be effective if mass production techniques could be developed. Clancy (1969) 
reported that the tachinid parasite Voria ruralis showed promise as a bioijogical control agent of the 
cabbage looper. Bryan et al. (1969) conducted studies on the role of temperature in development of 
Microplitis croceipes and selected 30°C as the optimal temperature for rearing this important parasite 
of Heliothis (s. lat.) species. Maltby et al. (1969) found a new species of Trichogramma that was 
adapted to the cereal leaf beetle, an introduced pest; they suggested that selective breeding of the 
parasite could improve its efficiency. Fye and Larsen (1969) conducted a preliminary evaluation of 
Trichogramma minutum as a biological control agent of lepidopterous pests of cotton. They found 
this species to be of little value because: 1) the rate of dispersion was slow and distances limited; 2) 
mortality of broadcast parasitized host eggs would be quite high, and timing of applications would be 
difficult; 3) searching capability of the wasps in complex situations was relatively poor; 4) longevity 
and ovipositional periods were short; and 5) high temperatures limit the activity of the adult female. 


Lewis (1970) described the life history and anatomy of Microplitis croceipes, a parasite of Heliothis 
(s. lat.) larvae, and Lewis and Burton (1970) described a rearing procedure for this parasite. Lingren 
et al. (1970) evaluated host and host age preference of Campoletis flavicincta (as perdistinctus) to 
determine the most appropriate host for use in mass rearing. Graham (1970) studied parasitization of 
several lepidopterous pests by Trichogramma semifumatum in the Lower Rio Grande Valley of 
Texas and reported that, though T. semifumatum is an important mortality agent in tomato and corn, 


30 


demand for insect-free produce mitigated against their use. The importance of 7. semifumatum in 
cotton was difficult to measure because of insecticide use. Ridgway et al. (1970) developed a mass 
rearing system for the common green lacewing (Chrysoperla carnea). Hoffman et al. (1970) reported 
on techniques for collecting, holding, and determining parasitism of lepidopterous eggs. Jackson et 
al. (1970) reported on the developmental biology of Leschenaultia adusta, a tachinid fly attacking the 
saltmarsh caterpillar, and suggested spraying laboratory-produced parasite eggs in the field. Bryan et 
al. (1970) reported on a comparison of two species of Eucelatoria, tachinid flies parasitic on 
Heliothis s. lat. Stoner (1970) studied the plant-feeding behavior of the predaceous bug Geocoris 
punctipes. Parker (1970) studied the seasonal mortality of the imported cabbageworm and the effect 
of introducing Trichogramma evanescens. This was the initial study for a later biological control 
program using 7. evanescens (discussed below). Schmidt (1970) also studied the biology of T. 
evanescens. | 


ARS scientists also began to realize that environmental manipulation strategies could play an 
important role in biological control. Reed et al. (1970) suggested that the lower numbers of brown 
soft scale found on citrus trees near windbreaks, could, in part, be due to increased efficiency of 
parasites when they are sheltered from the wind. 


Parker and Pinnell (1971) studied several species of Trichogramma to determine if and how they 
overwintered in Missouri. Day et al. (1971) studied the distribution of Microctonus aethiopoides and 
M. colesi, two important parasites of the alfalfa weevil, in the eastern U.S. McCoy and Selhime 

(197 1a, b) studied the influence of natural enemies, including the parasite Cheiloneurus inimicus, on 
black scales (Saissetia spp.) on citrus in Florida. Butler and May (1971) studied feeding of the 
common green lacewing on eggs of Heliothis (s. lat.) spp. Stoner and Surber (1971) studied the 
influence of temperature on the development of Anaphes iole (as ovijentatus), an egg parasite of 
Lygus hesperus. Lewis and Jones (1971) began their reports of studies on semiochemicals with a 
publication on the kairomone from Heliothis (s. lat.) spp. that stimulates host-seeking by Microplitis 
croceipes. Elsey and Stinner (1971) studied the biology of Jalysus spinosus, a predaceous stilt bug 
found in tobacco. Arbogast et al. (1971) reported on the developmental stages of the warehouse 
pirate bug (Xylocoris flavipes), an important predaceous bug in the stored product environment. 


In late 1964, ARS established the Biological Control of Insects Research Laboratory (BCIRL) at 
Columbia, MO, under the direction of F. R. Lawson. The primary project until Lawson's retirement 
in 1971 was biological control of pests of cabbage and other cole crops, including the imported 
cabbageworm, cabbage looper, diamondback moth, and green peach, cabbage and turnip aphids. This 
research is particularly interesting because it combined parasite importation, periodic releases, the 
use of both parasites and pathogens, and environmental manipulation techniques (Parker et al. 1971; 
Parker 1971). In this program two imported parasites, Trichogramma evanescens and Cotesia 
(=Apanteles s. lat.) rubecula, were released periodically in cabbage along with fertile hosts, the 
imported cabbageworm. The goals of the program were to: 1) introduce more effective parasites, 2) 
increase parasite density and synchronize parasite populations with host populations, and 3) increase 
host density to insure an adequate host supply for maintaining continuity of the parasites. These 
experiments resulted in 96% of the cabbage plants in treated plots producing grade A, No. | heads, 
whereas none of the plants in control plots produced marketable heads. A naturally-occurring 
"polyhedrosis virus", prepared by grinding as few as four infected looper larvae per acre, along with 
Trichogramma parasitization, controlled 100% of the cabbage loopers (Parker 1971). The bacterial 
insecticide, Bacillus thuringiensis, was also used to control the lepidopterous pests (Biever et al. 
1994). The aphids were normally controlled by parasites, predators, and pathogens in the absence of 
chemical pesticides (C. J. DeLoach, unpublished data). This program was an excellent example of 
how a variety of biological control approaches could be integrated into an effective Integrated Pest 
Management (IPM) program. Variations of this IPM program were successfully demonstrated at 
several commercial vegetable farms in Missouri (Biever et al. 1994), but a final pilot field test that 


31 


would have demonstrated the practicality of the program to producers was never carried out in 
Missouri. The mission of the Columbia laboratory was altered under its new Director, C. M. Ignoffo, 
in 1971; i.e., soybean insects became the new targets for biological control research, with emphasis 
placed on insect pathology. However, a highly effective biological control-IPM program for insect 
pests of cabbage, based on these early studies, was later developed and implemented in Washington 
and Texas (Biever et al. 1994); see Chapter IV. 


There was also considerable interest in the use of the predaceous larvae of the common green 
lacewing for augmentation programs during this period. Lingren et al. (1968) and Ridgway and Jones 
(1968, 1969) demonstrated the effectiveness of augmentative releases of the lacewing for suppressing 
Heliothis (s. lat.) spp. in cotton. However, the number of lacewing larvae required to suppress 
Heliothis (s. lat.) below the economic injury level was nearly 1 million/ha. These tests culminated in 
a series of releases in small plots at rates of 227 to 494 thousand larvae/ha where a peak Heliothis (s. 
lat.) spp. larval population of 44,460/ha was reduced 96% and cotton yield increased three-fold over 
the untreated check. From other small plot studies, the researchers concluded that releases of 123,000 
predator larvae/ha might provide effective control of Heliothis (s. lat.) spp. in cotton. The need for 
such large numbers again pointed out the need for improved rearing systems for biological control 
agents. Rearing of common green lacewing was reviewed by King and Morrison (1984) and 
Nordlund and Morrison (1991). 


One of the major impediments to economical inundative release programs is the high cost of 
producing sufficient numbers of insects. A major factor in the production cost is the necessity of 
producing large numbers of hosts or prey. This realization led to efforts to develop in vitro rearing 
techniques for parasites and artificial diets for predators. ARS efforts to develop artificial diets for 
predators includes those of Vanderzant (1969, 1973), who developed an artificial diet for larval and 
adult common green lacewings. This diet worked, but the presentation system was inefficient. Efforts 
to develop an encapsulation device were only somewhat successful (Anonymous 1971; Martin et al. 
1978), as the equipment was quite costly and cumbersome. Sterility of the diet was also a problem. 


Elsey studied the predaceous stilt bug Jalysus spinosus in tobacco in North Carolina (Elsey 1971, 
1972, 1974, 1975; Elsey and Stinner 1971). Although tobacco budworm populations were not 
reduced, some suppression of tobacco hornworm populations did result from early season releases of 
this insect. 


Hart (1972) tested Microterys flavus, an encyrtid parasite of brown soft scale, in citrus groves in the 
lower Rio Grande Valley of Texas. Apparently, this parasite and other natural enemies were largely 
eliminated by insecticide drift from nearby cotton fields. When chemical treatment was stopped and 
M. flavus was released inoculatively, biological control of the brown soft scale was reestablished. 


Lewis et al. (1971) demonstrated that Trichogramma evanescens perceived chemicals left by adult 
moths near oviposition sites, as first demonstrated by Laing (1937), and in 1972 they reported that 
moth scales were the source of a kairomone that stimulates host-selection behavior by this parasite. 
These studies resulted in considerable and continuing interest in the roles played by semiochemicals 
in the host- and prey-selection behavior of parasites and predators. 


In conclusion, the period 1953-72 saw an increased interest in the development of alternatives to 
conventional pesticides, including the augmentation and conservation of parasites and predators. 
Much of the work conducted by ARS scientists during this period involved basic biological and 
ecological studies of potential biological control agents. At least two studies demonstrated the 
technical feasibility of augmentation. One involved the use of the parasites Trichogramma 
evanescens and Cotesia rubecula against imported cabbageworm in cabbage (Parker et al. 1971, 
Parker 1971), and the other involved the use of the predator common green lacewing against 


32 


Heliothis (s. lat.) spp. in cotton (Ridgway and Jones 1968, 1969). These programs demonstrated the 
need for improved rearing techniques, particularly the need for artificial diets. Studies on 
semiochemicals influencing the host and prey selection behavior of entomophagous insects also 
began during this period; continuing research in this area is discussed in Chapter IV, section B.1.b. 


2. Arthropod-Parasitic Nematodes. By W. R. Nickle, J. R. Coulson, and P. V. Vail 


With the establishment of the Agricultural Research Service (ARS) in 1953, the old Bureau of Plant 
Industry, Soils, and Agricultural Engineering was abolished and much of its research functions was 
placed into the newly formed Crops Research Branch. This Branch was raised to Division status in 
1957 and its name was changed to Plant Science Division late in this period. Nematology 
Investigations, under the leadership of A. L. Taylor (1956-64) and J. M. Good (1964-72), continued 
as a unit of this Division's Crops Protection Research Branch. See also section C below on biological 
control of plant nematodes. 


In 1954, a nematode from the codling moth was found by ARS insect pathologists (Dutky and Hough 
1955) in the U.S., and was designated by an accession number "DD-136." The same species was 
found from the codling moth in the same year in Europe, where it was described as Neoaplectana 
carpocapsae. This nematode, now known as Steinernema carpocapsae, has many insect hosts and is 
known to vector a bacterium that kills the host. S. R. Dutky worked on this nematode-bacterium 
association for many years at the ARS Insect Pathology Pioneering Laboratory at Beltsville, MD. 
Early work in the 1950s and early 1960s and subsequent research by ARS and university 
nematologists in the U.S. and by foreign researchers, led to the eventual commercialization of this 
nematode by private companies in the 1980s. It is currently the most widely used nematode for insect 
control in the U.S. and throughout the world. (Poinar 1979; Nickle 1984; and references therein.) 


ARS studies with other nematodes for insect control during this period concerned nematodes 
attacking the face fly (Stoffolano and Nickle 1966; Nickle 1967), and mosquitoes (Chapman et al. 
1967; Petersen et al. 1968, 1969; Chapman 1974; Petersen and Willis 1972; Nickle 1972), and 
discovery of a new mermithid species (Filipjevimermis leipsandra) attacking cucumber beetles 
(Diabrotica spp.) (Cuthbert 1968; Poinar and Welch 1968). Host ranges of mermithid nematodes 
infecting mosquitoes as well as preliminary mass production methods for those organisms were 
developed by Petersen et al. (1969) and Petersen and Willis (1972). Work on the mosquito nematode 
(Romanomermis culicivorax) led to the development of the first commercial use of nematodes for 
pest control in the 1970s. It was also not until after 1972 that the first importations of exotic 
nematodes were made into the U.S. for insect control (see Chapter IV). 


Considerable advances were made during 1953-72 in the systematics of insect-parasitic nematodes; 
see Poinar, 1979, and Nickle, 1984. In 1965, W. R. Nickle joined the Nematology Investigations unit 
at Beltsville, MD. His efforts were to be concentrated on the systematics of insect-parasitic 
nematodes and their use in biological control of pest soil insects. 


3. Arthropod Pathogens. By P. V. Vail, J. R. Coulson, J. R. Adams, and H. Shimanuki 


In the late 1940s and early 1950s, E. A. Steinhaus, one of the preeminent leaders in the development 
of insect pathology in the U.S., began research, teaching and graduate programs in insect pathology 
at the University of California. He was a stong proponent of both basic and applied insect 
pathology/microbial control research. In the early to mid-1950s, his graduate students expanded the 
base of insect pathology in the United States and throughout the world, and these graduates in turn 
trained the "second generation" of insect pathologists. These developments led to the acceptance of 
insect pathology as a discipline within biological control. This, combined with the foresight of E. F. 
Knipling, Director of the ARS Entomology Research Division, led to establishment of insect 


33 


pathology/microbial control programs at many ARS laboratories throughout the United States. 
During these years, significant advances were made in both basic and applied insect pathology. 


One of the first actions taken by the newly formed Entomology Research Division was the creation in 
1954 of the Insect Pathology Pioneering Research Laboratory at Beltsville, MD. The Insect 
Pathology Unit of the Japanese Beetle Laboratory at Moorestown, NJ, was moved to Beltsville as 
part of this new Laboratory, which was headed by C. G. Thompson (1953-1961). Subsequent leaders 
of the unit, later called simply Insect Pathology Laboratory (and yet later Insect Biocontrol 
Laboratory), were A. M. Heimpel (1961-1979) and J. L. Vaughn (1979-present). The purpose of this 
Laboratory was to conduct basic research in support of more applied insect pathology/microbial 
control programs at the ARS field locations. 


Similar units devoted specifically to insect pathology research had already been established in the 
University of California at Berkeley in 1945 by Steinhaus, and in Canada in 1950 by J. W. M. 
Cameron. 


Research on honey bee diseases and their control continued in the Entomology Research Division's 
Apiculture Research Branch (briefly the Beekeeping and Insect Pathology Section) at locations in 
Beltsville MD, Laramie, WY, and elsewhere. Techniques were developed for controlling pests and 
diseases of the honey bee at Beltsville, MD (Cantwell and Lehnert 1968; Cantwell and Smith 1970; 
Cantwell et al. 1972). The first record of chalkbrood in the alfalfa leafcutting bee in North America 
was reported by Baker and Torchio (1968) at Logan, UT. Chalkbrood in the alkali bee was also 
studied (Batra and Bohart 1969). Tylosin lactate was discovered as a treatment for American 
foulbrood (Hitchcock et al. 1970) and methods to control other bee diseases were investigated 
(Moffett et al. 1969). New application techniques to enhance the efficacy of foulbrood control agents 
were developed (Wilson et al. 1970, 1971; Wilson and Elliott 1971). A diagnostic service for bee 
diseases was established during this period at the Beltsville laboratory, and continues to the present 
day. (See Beltsville laboratory's research in Appendix II.) 


Research on insect pathogens was also initiated during this period at other ARS locations under the 
administration of several Research Branches of the Entomology Research Division. In the 1950s, 
studies were begun by ARS researchers at Brownsville, TX, and Whittier (later Riverside), CA, on 
insect viruses, and at Ankeny, IA, and Mississippi State, MS, on other pathogens. In the 1960s, 
research on the bacterial pathogen Bacillus thuringiensis (Bt) was begun at the Brownsville station, 
through the research of H. T. Dulmage from 1960 to the 1980s. Over 1,000 isolates of Bt were 
purified, propagated, and tested for efficacy. These isolates are now in a collection at the ARS 
laboratory in Peoria, IL (Dulmage and Beegle 1982). Dulmage was also deeply involved in the 
development of standardization of commercial Bt formulations based on comparison with an industry 
accepted standard (Dulmage 1973 a and b). Various other pathogens were studied at other 
Entomology Research Division locations in Arizona, California, Florida, Illinois, Missouri, Montana, 
South Dakota, and Texas (see Appendix II). 


In 1957, research at Ankeny, IA, showed the deleterious effects of the protozoan pathogen Nosema 
pyrausta on populations of the European corn borer, including reduced fecundity of adults (Zimmack 
and Brindley 1957; Lewis et al. 1971); occasionally, negative impacts on beneficial insects were 
noted. Also at Ankeny, the fungus Beauveria bassiana was shown to reduce corn borer populations 
to near 90% (York 1958). Beginning in 1961, research at Peoria, IL, emphasized fermentation 
systems for production of Bacillus popilliae spores; although vegetative cells could be produced, 
they were not successful in producing spores. At Peoria, several techniques led to successful 
sporulation (Rhodes et al. 1965); however, development of high sporulation rates remain an enigma 
to insect pathologists and microbiologists today. 


34 


Early ARS tests with nuclear polyhedrosis viruses (NPVs) using spray and autodissemination 
techniques were conducted in southern California (Elmore 1961; Elmore and Howland 1964). ARS 
and University of California scientists conducted extensive studies on a virus isolated from the citrus 
red mite over a period of about 14 years. These studies included characterization (Smith et al. 1959; 
Reed and Hall 1972; Reed and Desjardins 1982). Also studied were methods of transmission (Reed 
et al. 1975) and potential methods of use (Gilmore and Munger 1963; Reed et al. 1973). 


Intensive studies were conducted at Brownsville, TX, in the 1960s to develop NPVs infectious to the 
Heliothis/Helicoverpa complex and cabbage looper as microbial control agents (Ignoffo 1964, 1965a 
and b, 1965b, 1966d, 1973). These and later studies (Ignoffo et al. 1965; Ignoffo 1966a and b and c; 
Ignoffo and Couch 1981) led to the first registration of a baculovirus for agricultural use. Of 
importance was that newly developed artificial diets (Vanderzant et al. 1962) for the host insect were 
utilized for mass production of the virus. As a part of a project for area-wide suppression of the boll 
weevil, McLaughlin (1962) demonstrated that Beauveria bassiana could infect overwintering insects 
when applied to hibernation sites. Several protozoan pathogens of the boll weevil were also studied 
during this period (e.g., McLaughlin 1967). Granular formulations of Bacillus thuringiensis provided 
the stimulus to develop this organism for European corn borer control (Raun, 1963; Raun & Jackson, 
1966). Lists of parasites and pathogens of mosquitoes, including viruses, protozoa, and nematodes, 
were developed at ARS laboratories at Lake Charles, LA, Gainesville, FL, Kerrville, TX, and Fresno, 
CA. 


Successful use of Bacillus thuringiensis B-exotoxins led to methods of reducing populations of horn 
fly larvae infesting cattle dung and also adult fly populations on range cattle (Gingrich 1965; 
Gingrich and Eschle 1966, 1971). Sutter and Raun (1966, 1967) were the first to show that B. 
thuringiensis crystals damage insect midgut cells allowing the contents to enter the hemocoel causing 
septisemia. Control of the corn earworm and fall armyworm with NPVs was investigated by Young 
and Hamm (1966) and Hamm and Young (1971). NPVs were found to be of two types, either with 
the capsids embedded singly or in multiples in the polyhedron matrix (Heimpel and Adams 1966). A 
number of other viruses were also described by scientists in the Insect Pathology Pioneering 
Laboratory and other ARS laboratories during this period. 


Two new microsporidians and a poxvirus were described from grasshoppers (Henry and Jutila 1966; 
Henry 1967, 1969a, 1971b; Henry et al. 1969). These pathogens would later be developed as 
microbial control agents for rangeland grasshoppers. Nosema locustae was eventually registered for 
this purpose by the Environmental Protection Agency (see Chapter IV). The manifold effects of a 
cytoplasmic polyhedrosis virus on cabbage looper was determined (Vail et al. 1967). A 
multiply-occluded NPV was isolated having a broad host range for many lepidopterous pests (Vail et 
al. 1971). This virus is a candidate as a microbial control agent and is now used extensively in 
medical research. A number of pathogens were reported from Coleoptera and were field tested at 
various locations (Daum et al. 1967; McLaughlin 1967; McLaughlin et al. 1967; Cuthbert 1968). 
Early studies on the impact of Beauveria bassiana on mosquitoes was demonstrated (Clark et al. 
1968). Extensive studies on ultrastructure, taxonomy, basic pathology, and transmission of 
protozoans infectious to lepidopterous and coleopterous postharvest pests were determined at Fresno, 
CA (Kellen and Lindegren 1968, 1971). A landmark discovery was made when "species" of 
Thelohania in larval and Nosema in adult mosquitoes were found to be the same species (Hazard and 
Weiser 1968). A pathogenic strain of Bacillus cereus was isolated from the cigarette beetle 
(Thompson and Fletcher 1972). In 1968, the ARS fire ant project began and included a component 
for the development of microbial control agents. Cell cultures from various insects, but primarily 
Lepidoptera and Orthoptera, were being established at numerous ARS laboratories to facilitate basic 
and applied research on pathogens. 


39 


Basic studies on the chemistry, characterization and mode of action of Bacillus thuringiensis led to 
further understanding of this and related bacterial pathogens (Faust and Dougherty 1969; Faust et al. 
1971 a and b). At Manhattan, KS, intensive studies were conducted on B. thuringiensis metabolism, 
origin and function of parasporal crystals and spore coat proteins (Bulla et al. 1970 a and b, 1971 a 
and b; Bulla and St. Julian 1972 a and b). Significant reductions of grasshopper field populations by 
the use of Nosema locustae were demonstrated (Henry 1971a) and the known host range of this 
protozoan was expanded to include 58 species of grasshoppers and other Orthoptera from throughout 
the world (Henry 1969b). Formalin was found to be an excellent antiviral agent for a number of 
viruses (Ignoffo and Garcia 1968; Vail et al. 1968; Bullock et al. 1969). Studies of viruses of stored 
product insects were initiated by Hunter at the Fresno location (Hunter and Dexel 1970; Hunter and 
Hoffmann 1970). Complete and continued replication of baculoviruses, as well as titration methods 
and cell line nutritional requirement studies were reported by scientists of ARS Arizona and 
Beltsville laboratories (Goodwin et al. 1970; Vail et al. 1973; Hink and Vail 1973). These were the 
first studies to show complete replication of baculoviruses as well as end point and plaque assay 
procedures, important to further studies on the molecular biology of these organsisms. 
Entomophagous insects such as sarcophagid flies as well as birds were demonstrated to disseminate 
occlusion bodies of a nuclear polyhedrosis virus (Hostetter and Biever 1970). The first RNA virus 
(crystalline array) was isolated from an arthropod, the twostriped grasshopper (Jutila et al. 1970). 


The "Heliothis NPV" (i.e., the NPV of corn earworm) was registered in 1970 by the U.S. Food and 
Drug Administration, the first baculovirus to be registered and mass produced for commercial use, 
and was registered by the Environmental Protection Agency in 1975 (Benz 1986). A summary of the 
research and development of this virus is provided by Ignoffo (1973) and Ignoffo and Couch (1981). 


The pink bollworm, cotton leafperforator and diamondback moth were reported as hosts of the alfalfa 
looper NPV (Vail et al. 1971, 1972). The serious effects of ultraviolet light on persistence of 
baculoviruses was demonstrated (Bullock 1967; Bullock et al. 1970). A significant increase in basic 
knowledge of the inactivation of microbials by sunlight led to a number of protectants to stabilize 
microbial pesticides (Ignoffo and Batzer 1971). A pioneering study on the influence of Rickettsiella 
on the navel orangeworm was conducted by Kellen et al. (1972). 


Research progress at ARS stations listed above, as well as in all other ARS locations where insect 
pathology research was initiated in the 1970s and 1980s after elimination of the Entomology 
Research Division, is discussed in Appendix II, arranged by location. For general information on the 
history of insect pathology during 1953-72, see Sweetman 1958; Steinhaus 1964; Hall 1964; Burges 
and Hussey 1971; Heimpel 1974; and references cited therein. 


B. BIOCONTROL CONTROL OF WEEDS. By J. R. Coulson and L. A. Andres 


As noted in the section A.1.a, research on natural enemies of weeds was included in the program of 
the ARS Insect Identification and Parasite Introduction Research Branch (IIPI). As such, research in 
this area commenced at the ARS European Parasite Laboratory in 1947. Target weeds at the EPL 
during 1953-59 included Klamath weed (or common St. Johnswort) (1953), gorse (1953, 1956-59), 
tansy ragwort (1956-59), Scotch broom (1956-59), Mediterranean sage (1956-59), Dalmatian 
toadflax (1956-59), Italian thistle (1956-59), puncturevine (1957-59), and hemp broomrape and 
Canada thistle (1959). 


In 1959, weed projects shifted to the new laboratory in Italy, see below. Shipments of natural 
enemies of several of these weeds were sent to the ARS station at Albany, CA, and to Hawaii in 
some cases. Results of the Klamath weed project are discussed in Chapter II. 


36 


Since most of these California weeds were believed to be of Mediterranean origin, work was phased 
out at the laboratory in France and shifted to a new ARS Biological Control of Weeds Laboratory 
established by L. A. Andres in Italy in 1959, which was developed specifically for the weed work. 
Directors of this laboratory during this period were L. A. Andres (1959-64), K. E. Frick (1965), B. D. 
Perkins (1965), and P. H. Dunn (1965-72). During 1959-72, target weeds at this new IIPI laboratory 
included over a dozen weeds common to the western states, including: gorse (1959-60), puncturevine 
(1959-62), Scotch broom (1959-66), Italian and slenderflower thistles (1959-60, 1966-67), other 
carduine thistles (1959, 1963-65) with concentration on musk thistle (1966-72), Dalmatian toadflax 
(1959-69), Mediterranean sage (1959-72), tansy ragwort (1961-66), cruciferous weeds (1966-68), 
and Russian thistle (1967-72). The laboratory in Italy was under the administrative and technical 
direction of IIPI's Beltsville, MD, and Albany, CA, offices, respectively. 


Concurrent with the initiation of weed work at the EPL, a station was established by IIPI in Iran, in 
1956, to study natural enemies of the poisonous western rangeland weed, halogeton, in Iran and 
Afghanistan. This station was headed by G. B. Vogt (1956), C. J. Davis (1957), and J. J. Drea 
(1957-59). Despite extensive surveys, good study populations of the weed could not be found, and 
the station was moved to Morocco in 1959, where research continued through 1962, under J. J. Drea. 
The most promising natural enemy, a moth species, studied during this period was found to be 
unsuitable for introduction into the U.S. 


Additional surveys for natural enemies of western rangeland weeds were made by ARS explorers in 
the USSR in 1965 under the auspices of a U.S.-USSR scientist exchange program (Coulson 198 1a), 
and in India, Pakistan, Egypt, Israel, Poland, and Yugoslavia as a result of the Special Foreign 
Currency (or PL-480) program discussed above. 


Most of the natural enemies found during overseas studies to be promising control agents of these 
western weeds were sent primarily to the newly constructed ARS Biological Control of Weeds 
Research Laboratory and quarantine facility at Albany, CA, for further evaluation. Directors of IIPI's 
Biological Control of Weeds Investigations and the Albany weed laboratory during this period were 
J. K. Holloway (1953-64) and L. A. Andres (1964-72). Some natural enemies of thistles were sent to 
Virginia; see below. 


In 1957, an interagency Subcommittee (later Working Group) on Biological Control of Weeds was 
established by the joint Weed Committees of the USDA and U.S. Department of Interior. This was 
done at the request of biological control of weed researchers who recognized the need for wide 
discipline participation in making decisions regarding selection of appropriate test plant species and 
the safety of introductions of foreign natural enemies of weeds. This group recommended plant 
species to be included in pre-release safety studies, reviewed detailed results of studies prior to 
recommending approval of proposed releases, and also provided comments on whether conflicts of 
interest existed concerning the targeted weeds. (Klingman and Coulson 1982-83; Coulson and Soper 
1989; Coulson 1992a.) 


Significant accomplishments of the research on eland weeds during 1953-72 included the 
establishment in the U.S. of a number of insect natural enemies of Canada, milk, musk, plumeless, 
and Italian thistles, tansy ragwort, gorse, Scotch broom, Mediterranean sage, and puncturevine. The 
success of the Klamath weed project extended into the early part of this period. Of the new target 
weeds, the most successful results were obtained on tansy ragwort, musk thistle, and puncturevine. 


Tansy ragwort is a poisonous European weed in pastures and rangeland of the northwestern U.S. The 
ARS research on this weed was carried out primarily at the Albany laboratory (J. K. Holloway, L. A. 
Andres, K. E. Frick, R. B. Hawkes), the Paris laboratory (H. L. Parker), and the Rome laboratory 

(L. A. Andres, K. E. Frick). A total of three European insects were successfully introduced for 


a” 


biological control of tansy ragwort in the United States. Two of these, the cinnabar moth (Tyria 
jacobaeae) and the "ragwort flea beetle" (Longitarsus jacobaeae), have been primarily responsible 
for excellent control of this weed. A third insect, the "ragwort seed fly" (Botanophila seneciella), 
was first introduced in 1966 and successfully established in some areas, but its impact is largely 
unknown. Initially, the leaf- and flower-feeding cinnabar moth, released in 1959, provided some 
relief, but it was not until the release of the root- and leaf-feeding beetle, beginning in 1969, that 
dramatic control of this weed occurred. Tansy ragwort has been reduced to less than 1% of its former 
densities at study sites in northwestern California and western Oregon (the only areas where impact 
studies have been carried out). The replacement vegetation has been chiefly native plants and more 
benign weeds. In Oregon alone, the savings from the control of tansy ragwort have amounted to ca. 
$5 million annually, with an estimated cost:benefit ratio of 1:14. Field evaluation studies were 
carried out in California by ARS personnel, and in Oregon by personnel of Oregon State University 
and the Oregon Department of Agriculture. (See references cited below.) 


Musk thistle is a serious pest of pastures and rangelands throughout the U.S. Much of the domestic 
research on the musk thistle insects received from the ARS laboratory in Europe was funded under a 
cooperative agreement with scientists of the Virginia Polytechnic Institute and State University 
(VPI). A European seed weevil, initially released in Canada, was tested by ARS scientists and 
disseminated and established throughout the U.S. from European and Canadian stock, and later from 
populations initially established in Montana and Virginia. The weevil effected substantial reduction 
of musk thistle populations in many locations, and had additional effects on plumeless, milk, and 
Italian thistles. However, testing began on additional insect enemies of these thistles deemed required 
for better control, and these were eventually introduced during the next period (1972-93). 


Puncturevine is an introduced spiny weed of roadsides, cultivated crops, pastures, and rangeland 
throughout most of the U.S. Two species of European weevils were successfully introduced from 
Italy and have established and spread in California and southwestern and central states from Texas 
north to Nebraska. Of 57 puncturevine-infested California counties surveyed in 1975, 32 reported a 
major decrease in puncturevine populations as a direct result of the weevils. This represents an 
estimated annual savings in treatment costs for California alone of $1,700,000. The overall one-time 
cost of the puncturevine project was estimated to be $360,000, one-fifth of the resulting annual 
benefits. 


For references to research results for rangeland weeds during this period, see Parker 1960; Frick and 
Holloway 1964; Frick and Andres 1967; Frick 1969, 1970 a and b, 1978; Andres and Goeden 1971; 
Kok and Surles 1975; Rees 1977; Goeden 1978; Hawkes and Johnson 1978; Maddox and Andres 
1979; Batra et al. 1981; Hawkes 1981; Huffaker et al. 1983; Piper 1986; Julien 1987, 1992; 
Pemberton and Turner 1990; McEvoy et al. 1991; Isaacson and Radtke 1993; Andres and Rees 1995; 
Turner and McEvoy 1995. 


Beginning in 1959, ARS pioneered a new thrust in biological control, the biological control of 
aquatic weeds. Since 1899, the U.S. Army Corps of Engineers has been charged with the 
responsibility of controlling aquatic weeds in the nation's navigable waterways; these activities were 
expanded in 1945. As part of these expanded efforts, the Corps of Engineers began in 1959 to fund 
ARS research to explore the feasibility of biological control of alligatorweed and waterhyacinth, two 
of the most serious weeds of waterways in the southeastern U.S., and subsequently has funded such 
research involving other aquatic weeds. Working under the technical direction of the ARS Albany 
laboratory, an IIPI taxonomist, G. B. Vogt, conducted surveys for natural enemies of these two weeds 
in South America, their original homeland, during 1960-62, and an ARS laboratory was established 
by D. M. Maddox in Argentina in 1962 to study further the promising insect enemies found. IIPI 
entomologists in charge of the Argentine lab were D. M. Maddox (1962-67), B. D. Perkins 
(1968-71), and C. J. DeLoach (1971-72). An SFC (PL-480) project to study the biologies of the 


38 


natural enemies of these weeds in Uruguay was also established. Three insect enemies of 
alligatorweed were introduced and established in the U.S. in 1964-71; prior quarantine studies, initial 
domestic field releases and subsequent evaluation studies were conducted by scientists from the ARS 
Albany, CA, laboratory. In 1970, IIPI established the Insect Enemies of Aquatic Weeds Laboratory at 
Gainesville, FL, with N. R. Spencer in charge, to conduct further research on the biological control 
of these and other aquatic weeds in the Southeast. In 1972, IIPI stationed an entomologist (B. D. 
Perkins) at USDA's Aquatic Weeds Research Laboratory at Fort Lauderdale, FL, to handle release 
and evaluation of natural enemies of both alligatorweed and waterhyacinth in Florida. Two of the 
introduced alligatorweed insects spread rapidly throughout the southeastern U.S., with spectacular 
results in some areas, and in general causing a substantial reduction in alligatorweed infestations in 
many areas of the Southeast. An early (1976) and very conservative estimate of the benefits of this 
control of alligatorweed in terms of herbicidal treatments no longer required was $400,000 annually, 
at an estimated total cost of ARS research of $1 million. Results of a 1981-82 survey of 
alligatorweed in ten southern states conducted by the Corps of Engineers showed that of the 97,000 
problem acres of the weed in 1963, less than 1,000 problem acres remained in 1981 (Cofrancesco 
1993). The first of the natural enemies of waterhyacinth was not introduced (through the Albany 
quarantine facility) until 1973. 


Explorations for natural enemies of aquatic weeds were also conducted under the SFC or PL-480 
program in India, Pakistan, and Yugoslavia, the weeds involved being waterhyacinth and the 
submersed weeds Eurasian watermilfoil and hydrilla. The Weeds Investigations unit of the Crops 
Protection Research Branch, Crops Research Division, ARS, supported a number of these projects as 
did IIPI. There was considerable cooperation between these two research branches in the biological 
control of weeds research programs. 


For some references on the early aquatic weed research, see Andres and Goeden 1971; Maddox et al. 
1971; Perkins 1973; Spencer and Coulson 1976; Andres 1977; Coulson 1977. 


The successes obtained in the biological control of weeds program, including Klamath weed, 
alligatorweed and tansy ragwort, led to a marked expansion of effort in this area. As reported above, 
during 1959-72, two foreign laboratories (Italy and Argentina) and two domestic laboratories (for 
research on aquatic weeds) were established by the IIPI, and a new quarantine facility was 
constructed (in 1963) at Albany, CA, and the staff there increased to four scientists. At the time of 
the 1972 reorganization, plans were underway for additional IIPI laboratories, with quarantine 
facilities at Stoneville, MS, and Temple, TX, for biological control of southern pasture and row crop 
weeds, and brush and other weeds of southwestern rangelands, respectively. Similar efforts on 
northeastern weeds was not established until 1974. 


C. BIOLOGICAL CONTROL OF PLANT NEMATODES. By R. M. Sayre 


As noted in the above section A.1.2 on insect-parasitic nematodes in this Chapter, Nematology 
Investigations continued in the new ARS Crops Research Division, created in the 1953 
reorganization (name changed to Plant Science Division late in this period). The subsequent 20 years 
was the period of most rapid growth in numbers of nematologists at universities, in industry, and at 
federal laboratories. The demonstration of the economic importance of nematodes in crop production 
was made possible only by utilizing the newly discovered effective nematicides. These two factors 
became the driving force for the increase in numbers of nematologists. The demonstrated increase in 
crop yields in field plots that had been treated with nematicides was not overlooked by 
administrators. Some universities allowed formation of independent departments of nematology, 
while others permitted changes in the names of entomology and plant pathology departments to 
include nematology, and hired new personnel for these departments. In 1956, the USDA, partially in 
acknowledging the importance of nematicides in crop production and in recognizing A. L. Taylor's 


39 


leadership in nematicide development, named him leader of the Nematology Investigations, a post he 
held until his 1964 retirement. The Society of Nematologists was formed in 1961, and the first 
estimates of crop losses caused by nematodes were assembled and published by the Society 
(Feldmesser et al. 1971). 


The study of possible biological control agents of nematodes languished in the USDA at first. But 
some research activity in this area continued at universities. Culminating in 1965, the studies of 
Rodriguez-Kabana et al. (1965) were to report the first instances of biological control of a plant 
nematode which was mediated by a bacterium. 


The 1962 publication of Rachel Carson's book Silent Spring (Carson 1962) resulted in an increase in 
federal funding and an ensuing increase in numbers of federal nematologists. In 1965, under the new 
leadership of J. M. Good, eight new positions were created in the Nematology Investigations unit in 
order to meet the national need for finding methods of controlling nematodes other than reliance on 
chemical nematicides. Five positions, at scattered research stations in the U.S., were crop-oriented 
toward the nematode problems in their regions. The remaining three positions were allotted to 
Beltsville, MD. Two were filled by nematode taxonomists to study certain groups of nematodes (see 
section on insect-parasitic nematodes in this Chapter). The third was designated for research on the 
biological control of plant-parasitic nematodes, and was filled by R. M. Sayre. His research during 
this period considered the soil invertebrates (i.e., amoebae, tardigrades, and turbellarians) 
antagonistic to nematodes. Also, the use of sewage sludge as a soil organic amendment to control 
nematodes was investigated, as was the use of the water mold, Catenaria sp., as a possible biological 
control agent (Sayre 1971). 


In the late 1960s, additional USDA funds were made available as grants to universities and other 
research organizations. Three grants involving biological control of nematodes were made as 
follows: (1) R. Mankau, University of California, Riverside, who initiated a program that was 
eventually to lead to the discovery of at least two potential biological control agents; one was a 
promising bacterial disease of plant nematodes currently designated as a Pasteuria species, the other 
being a nematode-trapping fungus. (2) G. C. Smart, University of Florida, reexamined certain 
predaceous nematodes for their potential to control crop pest nematodes (Smart 1986). (3) D. C. 
Norton who began a program studying soil factors influencing nematodes, that led to the publication 
of "Ecology of Plant-Parasitic Nematodes" (Norton 1978). 


D. BIOLOGICAL CONTROL OF PLANT PATHOGENS. By G. C. Papavizas and R. J. Cook 


Biological control in plant pathology was born as a concept in the USDA in 1955. In the early part of 
that year, V. R. Boswell, Chief of the Vegetable and Ornamentals Research Branch of the new ARS 
Crops Research Division, submitted a proposal to the American Society for Horticultural Science 
(ASHS) suggesting the creation of a Committee of the Division of Biology and Agriculture with the 
subject of "Biological Control of Soil-Borne Plant Pathogens." The ASHS approved the proposal and 
submitted it to the Divison of Biology and Agriculture of the National Research Council on October 
3, 1955. The proposal contained information on the economic problem, description of more than 40 
soilborne plant pathogens, estimated annual expenditures by private farm enterprises for 
disease-control measures, technical problems, and a plan to work on cultural and biological control. 
Based on this proposal, the U.S. Congress appropriated a small amount of funds to perform research 
in ARS on soilborne plant diseases. Following the advice of Boswell, the Crops Research Division 
created at Beltsville, MD, the Mushroom and Microbiology Investigations, a new unit within 
Boswell's Branch, and appointed E. B. Lambert, a mushroom expert, as Investigations Leader. The 
Microbiology Group was composed of two scientists, C. B. Davey and G. C. Papavizas, who joined 
ARS in 1957, and was charged with the responsibility of developing a research program on soilborne 
plant pathogens. After publication of Rachel Carson's book "Silent Spring" (Carson 1962), additional 


40 


funds were added to the Microbiology Group in FY 1965. In 1966, Papavizas became Investigations 
Leader and recruited four more scientists, thus increasing man-years in the unit from 2.0 in 1957 to 
6.0 in 1966. Davey, who left ARS in 1962, was replaced by W. A. Ayers. Except for a change of the 
Division name from Crops Research to Plant Science Division late in the period, this organizational 
structure continued until 1972 when ARS underwent a major reorganization. 


The research of the Microbiology Group during this period centered on systems ecology of the 
harmful microbes that cause diseases on or through the root systems. The Group developed methods 
to isolate and enumerate several important and widespread soilborne plant pathogens from the soil 
and plant rhizosphere; advanced new and intriguing concepts in soil-microorganism-plant 
interactions, behavior of plant pathogenic organisms in soil, and fundamental principles on the 
manner in which organic and inorganic constituents influence the ecology and behavior of important 
plant pathogens; developed the theory of competitive saprophytic activity and its exploitation in 
enumerating and controlling Rhizoctonia; studied the impact of chemical agents on nontarget 
microorganisms; and unravelled the enzymatic mechanisms of Aphanomyces and Rhizoctonia 
instrumental in disease development. (Papavizas 1973.) 


While scientists of the Mushroom and Microbiology Investigations were studying systems ecology 
and laying the foundation for research to follow at Beltsville, a small group of ARS scientists at the 
Tidewater Research Station at Holland, VA, developed the "non-dirting" control of the peanut stem 
rot disease caused by Sclerotium rolfsii (Garren and Duke 1958). 


Meanwhile, USDA plant pathologists in the State of Washington were studying natural or induced 
suppression of soilborne plant pathogens by resident antagonists in soils, following up on earlier 
discoveries that biological control of such pathogens was most productively directed at enhancement 
of resident antagonists. ARS scientists at Prosser, WA, demonstrated that soils cropped repeatedly to 
potatoes under irrigation became microbiologically suppressive to common scab caused by 
Streptomyces scabies (Menzies 1959), and that soils of the Columbia Basin and Yakima Valley 
irrigation districts where common beans were grown ranged between extremes of highly favorable 
(conducive) and highly unfavorable (resistant or suppressive) to the bean root-rot pathogen, 
Fusarium solani f. sp. phaseoli (Burke 1965). In 1969-71, R. J. Cook and associates, ARS, Pullman, 
WA, demonstrated that a factor, associated specifically with soils from fields where wheat take-all 
disease had declined, could be transferred to and expressed in other fields (Baker and Cook 1974). 
This work at Pullman on biological control responsible for take-all decline was continued during 
1973-present (see Chapter IV). 


A major event during this period was the convening in 1963 at Berkeley, CA, of the First 
International Symposium entitled "Ecology of Soilborne Plant Pathogens - Prelude to Biological 
Control." The idea for this symposium grew from the activities of the ASHS Committee on 
Biological Control of Soilborne Plant Pathogens, mentioned above. (Baker and Snyder 1965). Of the 
40 papers, none were on introduced antagonists, the emphasis being instead on soils, plants, resident 
antagonists, and biological control through soil microbiologies and the plant. In contrast, the Sixth 
International Symposium on Ecology of Soilborne Plant Pathogens held in Kyoto, Japan, in 1988, 
covered this same range of topics, but in addition about half of the papers dealt in one way or another 
with specific antagonists manipulated or introduced for biological control purposes. 


Research on the biological control of foliar plant pathogens was initiated in 1970 at the ARS 
laboratory at Oxford, NC. This research continued and is discussed in Chapter IV, section E. 


4] 


Table 1. Benefits of Some USDA Classical Biological Control Programs, 1963-87'” 


eee eer errr renee — 





A B 
Acres Not Total Savings Year 
Pest States Infested Treated per Year Calculated? 
(X1000) 

Alfalfa weevil 18 5,767 85% * $ 48.9 million 1986 
Alfalfa blotch 10 2,049 100% > 13.2 million 1978 

leafminer 
Pea aphid (on 22 13,494 © 30% * 36.4 million 1984 

alfalfa only) 
Cereal leaf beetle 5 1,341 55% 7 14.0 million 1978 
Annual Savings ?$ 112.5 million 


' Prepared by W. H. Day, ARS Beneficial Insects Research Laboratory, Newark, DE, September 
1988. Benefits from promising projects still in early stages (e.g., euonymus scale, birch leafminer, 
tarnished plant bug) are not included. 


? 1993 savings (adjusted for inflation) would exceed $146,000,000. 


* The older data underestimate present savings considerably because of subsequent increases in crop 
value, cost of pesticides, and parasite and pest ranges. In terms of 1993 dollars, these figures are 
respectively: 63.7, 17.2, 47.3, and 18.2 million dollars, for a total of $146,400,000 annual savings. 


* Calculated as A X B X $10/acre, conservative costs of one insecticide treatment/year eliminated by 
biological control; savings due to reduced environmental damage are additional. For alfalfa weevil, 
see Table 2 and Day, 1981. 


* Damage is usually less than costs of control, so this figure is the average yield loss ($6.44/acre) that 
was prevented by the biological control of this pest. Infested area (and savings) is considerably larger 


in 1988. See also Hendrickson & Plummer, 1983. 


° 100% of acreage that formerly needed treatment in an average year. For pea aphid, savings to peas 
are additional but appropriate data have not been found. 


’ APHIS data for crop losses; parasite ranges are much greater in 1988, so savings are 
commensurately larger. See also Chapter VI below. 


42 


Table 2. Estimated Annual Savings to Farmers and Consumers from the Alfalfa Weevil 
Biological Control Program in the Northeastern United States’ 





A B AXB 
Acres of % Not Acres Net 
State? Alfalfa’ Treated‘ Not Treated Savings® 
(X1000) (X1000) 
ME pat 90 24.3 $ 243,000 
VT 115 90 103.5 1,035,000 
NH 19 90 tyra 171,000 
MA 30 90 27.0 270,000 
RI 3 90 yd 27,000 
CE 23 90 20,7 207,000 
NY 940 90 846.0 8,460,000 
PA 840 90 756.0 7,560,000 
NJ 45 90 40.5 405,000 
DE 7 90 6.3 63,000 
MD 80 80 64.0 640,000 
VA 88 50 44.0 440,000 
WV 100 80 80.0 800,000 
OH 600 90 540.0 5,400,000 
IN 420 80 336.0 3,360,000 
Is 800 70 560.0 5,600,000 
MI 1,400 90 1,260.0 12,600,000 
KY 230 70 161.0 1,610,000 
Totals 4,889.1 © $ 48,891,000 


' Prepared by W. H. Day, ARS Beneficial Insects Research Laboratory, Newark, DE, September 
1988. 


? States that primarily benefitted from the ARS program. Additional states to the west and south 


(recent APHIS program) are now experiencing increasing parasite impact, and are producing savings 


which are not included here. 
> For 1984 (1985 USDA data, most recent available; does not change much from year to year). 
4 Estimates (conservative) by W. H. Day, averages of 1985-86. 


> Calculated as A X B X $10/acre for insecticide and application costs; savings due to reduced 
environmental damage are additional. 


® $63,723,000 in 1993 dollars (adjusted for inflation); see Table 1. APHIS figures following their 
extensive parasite distribution program (Bryan et al. 1993) provide an increase in savings for the 
entire USDA alfalfa weevil biological control program to a total of an estimated $88,000,000 
annually, measured in 1987 dollars (Moffitt et al. [1990]). 


43 


CHAPTER IV 
1973-1993 
AGRICULTURAL RESEARCH SERVICE 


A. ORGANIZATIONAL CHANGES AND GENERAL EVENTS. By J. R. Coulson 


In 1972, the Agricultural Research Service (ARS) underwent a massive, far-reaching reorganization. 
The regulatory and control programs of ARS had already been removed in 1971 and placed in the 
newly formed Animal and Plant Health Inspection Service (APHIS). In 1972, the remaining research, 
discipline-oriented Divisions, including the Entomology Research Division and the Plant Science 
Division (previously Crops Research Division), were abolished. The many research units throughout 
the country and overseas, formerly administered by the several Research Branches of these 
Divisions, were placed administratively into 29 Areas in four Regions in the U.S., and an 
International Programs Division. The rationale for this reorganization was to enhance and increase 
multidisciplinary research, to bring management of research programs closer to area and regional 
problems, to increase cooperation between ARS and state experiment station scientists and other 
regional and local groups, and to eliminate a number of research administrative and support positions 
with a corresponding return of resources to productive research. To provide leadership and continued 
focus on the national aspects of ARS programs and to provide coordination of research by 
commodity, discipline, and program areas, a National Program Staff (NPS) was established, as were 
several other planning and coordinating bodies. 


A reorganization of such a broad scope was naturally controversial, and many serious doubts and 
questions were raised both within ARS as well as in outside scientific circles and in the U.S. 
Congress. There was, for example, considerable concern expressed over the effect of the elimination 
of entomology as a distinct entity in the USDA, a status it had held since the establishment of the 
first Division of Entomology in the Department in 1881. However, research programs within ARS 
continued with varying degrees of difficulty caused by adjustment to new administrative and 
coordination channels, an increase in paperwork at the scientist level (as a result of the loss of some 
administrative levels and increase in others), and the movement or loss of a number of senior 
scientists and science administrators (during the first year of the reorganization, 106 employees were 
transferred from the Washington, DC, and Beltsville, MD, administrative areas to the field, including 
34 former program administrators, and there were 99 retirements [U.S. House of Representatives 
1973]). ARS biological control programs were both positively and negatively affected by the 
reorganization. Classical biological control, with its need for close coordination of overseas 
exploration and domestic quarantine and field research aspects, was particularly badly affected; see 
sections B.1.a and C.1 below. 


Part of the reason for the negative impact on ARS biological control programs, at least in the 
beginning, was the fact that there was no Staff Scientist responsible for biological control on the 
National Program Staff until 1976, when D. E. Bryan was appointed to that position. That position 
was also given the responsibility for ARS research in insect taxonomy. Also, it was not until 1976 
that ARS National Research Program (NRP) documents were developed, for biological control as 
well as for other ARS research programs. The NRP documents outlined a 10-year plan describing 


44 


current technology in the various research program areas, identified national research objectives, 
described methods for achieving those objectives, and provided the accounting and reporting system 
by which those program areas were planned and managed. The responsibility for coordinating 
research for each NRP was assigned to a NPS Staff Scientist (later designated as National Research 
Program Leader). Though biological control was an integral part of the research of a number 
(initially 10) of NRPs, a special NRP (no. 20260) was established to deal with the exploration for, 
and introduction, augmentation, and conservation of biological agents for the control of insects, 
weeds, plant pathogens, and other pests, and for insect and mite taxonomy (USDA 1976a). 


Prior to the appointment of Bryan and establishment of NRP 20260, biological control matters were 
handled in the NPS by NPS Staff Scientists for weeds (W. B. Ennis) and bees (M. D. Levin). In 
addition, a number of Technical Advisors (TAs) were designated, first (1974) on a regional basis and 
later on a national basis, to assist NPS scientists in the planning and assessment of research and 
provide counsel on technical matters both to NPS and to ARS scientists and administrators in the 
field; there were nine TAs for the various aspects of biological control (for a list of TAs, see USDA 
1980b). The TA system was abolished in 1981. 


Recognizing the special coordination needs for biological control research, particularly in classical 
biological control, there was established in 1973 an ARS Working Group on Natural Enemies of 
Insects, Weeds, and Other Pests (WGNE); see section B.1 below on classical biological control for 
more detail on its establishment. ARS insect pathology programs continued to have informal 
coordination of activities by means of periodic research meetings. These meetings provided a 
mechanism for easy information exchange and development of cooperative research. Partly due to 
financial constraints, these meetings were no longer held after the mid-1980s. 


The WGNE consisted of two biological control specialists, of appropriate disciplines (including 
insect pathology), from each of the four ARS Regions, and a member from the International 
Programs Division, and was chaired by Drs. Ennis and Levin from 1973-75, and Dr. Bryan from 
1975 until his retirement in 1979. Liaison members were also appointed to represent APHIS, the 
Forest Service (FS), the Cooperative State Research Service (CSRS), and the Environmental 
Protection Agency (EPA). The WGNE Charter, as finalized at the first WGNE meeting, is presented 
in Appendix I.A. Some of the functions performed by the WGNE were: (1) establishment of 
priorities for research at the ARS overseas biological control laboratories; (2) assessment of 
biological control quarantine facility capabilities and needs; (3) recommendations on proposals for 
biological control explorations; (4) compilation of annual rosters of ARS biological control 
researchers; (5) preparation of annual reports of ARS biological control activities for the ARS 
Administrator and NPS; (6) preparation of ARS guidelines for introduction of exotic biological 
control agents, a still unfinished task (Coulson and Soper 1989; Coulson et al. 1991); (7) review and 
prioritization of proposals for foreign biological control explorations for funding from the ARS 
Administrator's foreign exploration funds; and (8) provision of solicited information and advice in 
many areas of biological control for the NPS. Similar biological control committees or working 
groups were established in the Southern and Northeastern Regions of ARS during the early years 
following the reorganization, which served coordination and information gathering and dissemination 
purposes within the regions and for the WGNE. These regional groups were disbanded with the 
abolition of the ARS Regions in late 1984. 


In 1976, in partial response to the Secretary's Memorandum No. 1890 concerning USDA's Program 
for Environmental Quality, an interagency Work Group on Biological Pest Control Agents 
(WGBCA) was established in the USDA under the aegis of USDA's Office of Environmental Quality 
Activities (OEQ), to provide assistance in formulating USDA policies and coordination in the area of 
biological control research. Membership of the WGBCA included representatives from the National 
Program Staffs of ARS and APHIS' Plant Protection and Quarantine (PPQ), and from CSRS, FS, the 


45 


Extension Service (ES), Economic Research Service (ERS), and the Office of General Counsel, and 
the Pesticide Coordinator from the Secretary's office. The ARS NPS Staff Scientist, D. E. Bryan, 
served as Chairman. The Charter of the WGBCA is presented in Appendix I.B. 


One of the WGBCA's first tasks was the organization of a federal-state task force that produced the 
1978 publication "Biological Agents for Pest Control - Status and Prospects" (USDA 1978). This 
publication highlighted a number of opportunities for expanded use of beneficial organisms for pest 
control, and included an appendix indicating the statutory authorities for the USDA to undertake 
research, education, or regulatory action on biological agents for pest control. As a direct result of 
one of the 11 major recommendations made and published by this task force, the ARS Biological 
Control Documentation Center, with its planned databases, was established in 1982 (Coulson 1988, 
1992b). As per the task force recommendation, the Documentation Center was developed to serve as 
"a national information storage and coordinating system specifically designed for assembling and 
collating domestic and international information relevant to all biological agents that might be used 
for pest control" and was designed to provide information for ARS and other biological control 
scientists and for the ARS National Program Staff. Many of the sections of this history of USDA 
biological control have been prepared from published and unpublished documents on file in the 
Center. 


Several interagency subcommittees were established by the WGBCA, including one to deal with 
evaluations of proposed introduced biological control agents (see section B.1 below on classical 
biological control), another to work with EPA and the U.S. Department of Interior in considering 
changes in conditions specified in Section 25(b) of the Federal Insecticide, Fungicide, and 
Rodenticide Act (FIFRA) concerning regulation of biological control agents, and a third to work with 
APHIS to draft proposed legislation concerning regulation of the importation of biological control 
agents. The WGBCA was disbanded when USDA's Office of Environmental Quality was abolished 
in 1981. , 

In late 1977-early 1978, ARS was part of another reorganization within the USDA which resulted in 
the establishment of a Science and Education Administration (SEA) encompassing the former 
agencies ARS, CSRS, Extension Service, and other units. The establishment of SEA was to reflect an 
equal emphasis for the major mission/activities of Federal and cooperative research, extension, 
teaching, and libraries, while simultaneously providing a strong focus addressing major national 
programs in these mission/activities, by means of an extensive joint program and planning staff 
composed of Federal and non-Federal personnel. The ARS became first "Federal Research" (FR) and 
later "Agricultural Research" (AR) under this new organizational structure; CSRS became 
"Cooperative Research" (CR). Another USDA reorganization in 1981 restored the previous 
organizational structure and AR became once more ARS. Other than changes in the top 
administration and in reporting procedures, etc., there was little effect of these reorganizations on 
AR/ARS research programs, including biological control. (A similar reorganization was announced 
in 1993; see below.) 


Also in 1978, another new agency was established in the USDA, the Office of International 
Cooperation and Development (OICD). Until that year, USDA's international programs were 
distributed among a number of agencies, including ARS' International Programs Division (IPD). 
OICD was established to improve the management of these programs. Since the 1972 ARS 
reorganization, IPD (later International Program Staff) had been responsible for administration of 
ARS' overseas laboratories, including those devoted to biological control, and had also administered 
the PL-480, or Special Foreign Currency Program, insofar as it related to ARS research. The latter 
was placed under OICD in 1978, together with many IPD personnel. OICD also became responsible 
for scientist exchange programs with a number of countries, through which many biological control 
exchanges have since taken place, beginning with several important exchanges with the People's 


46 


Republic of China (Wong 1982). See also Hedlund 1986, for other OICD programs of importance to 
biological control. (At the end of 1993, OICD became part of USDA's Foreign Agricultural Service.) 


In 1981, an International Activities (IA) office was established in ARS and administration of ARS 
overseas laboratories was placed under this office, along with responsibility for ARS international 
interests, and IPD was soon abolished. Supervisors of this office, and thus administrators of ARS' 
overseas laboratories, have been B. M. Kopacz (1981-86) and D. R. Kincaid (1986-91); R. S. Soper 
served as IA Director, in an acting capacity, from 1991 until his appointment as Assistant 
Administrator of the newly created Office of International Research Programs in 1992. 


One of the rationales for the 1972 reorganization was to effect an enhancement and increase in 
multidisciplinary research within ARS. That this was a successful outcome of the reorganization is 
reflected in the mixture of entomology, nematology, weed science, and plant pathology in the various 
biological control coordinating bodies established in ARS since 1972, from the mixture of these 
disciplines in the task force that developed the 1978 publication on biological control agents (USDA 
1978), and by the fact that the 1980 Beltsville Symposium on biological control was the first such 
symposium to bring together these four disciplines (Papavizas 1981; Cook 1981). Such a mixture of 
disciplines has been the case in subsequent biological control workshops and conferences, such as 
those of 1983, 1984, 1987, and 1991 noted below. 


After the 1979 retirement of D. E. Bryan, first NPS Staff Scientist for Biological Control and Insect 
Taxonomy, that NPS position was not immediately filled, its duties being temporarily carried out by 
M. T. Ouye. J. J. Drea was appointed to the NPS biological control position in October 1980 and 
served in that capacity until an NPS reorganization in late 1982. During 1979-82, NPS use of the 
WGNE languished; the last (sixth) meeting of the group having taken place in 1978, and the group 
was effectively dissolved by the end of 1982. 


Thus, by 1983, biological control was once again without focused representation on the NPS. 
Instead, an NPS Biological Control "Matrix Team" was established, one of many such NPS Teams 
established in 1983. The Team consisted of NPS specialists in plant pathology, weed science, and 
plant, man-and-animal, and post-harvest entomology. NPS scientists representing other areas were 
added at later dates. From 1983 to 1987, the Team was variously chaired by W. Klassen, R. D. 
Jackson, and J. E. Wright, none of whom were biological control specialists. The duties of the Team 
were to develop and implement a national research plan for biological control, provide scientific and 
technical coordination and leadership for the overseas and domestic biological control laboratories 
including identification and prioritization of research thrusts, and provide leadership and 
coordination of interagency biological control research activities. 


During 1983-87, there were several "adjustments" in the organization and management of ARS, 
including elimination of the four Regions and their administrative offices, and reduction in the 
number of Areas, first to 11 and later to eight, with their Directors reporting directly to the ARS 
Administrator, and the initiation of a totally new management system for ARS research. The NRPs 
established in 1976 were abolished, and a new ARS Program or Strategic Plan was formulated 
(USDA 1983a), which was followed by 6-Year Implementation Plans that were to be continuously 
updated (USDA 1983b, 1985). Research was to be managed even more strictly than before by CRIS 
(Current Research Information System) Work Units, which were to be developed by ARS scientists 
and approved by line administrators and the NPS, and which were grouped by the various research 
Approaches, Approach Elements, and Problems within the six ARS Objectives. The latest 
Implementation Plan, at this writing, was for 1992-1998 (USDA 1991). 


As a result of increasing concerns from public and scientific sectors about environmental 
contamination and the need for increased use of nonchemical methods of pest control, a number of 


47 


interdisciplinary workshops and conferences on biological control were held during 1983-87, which 
brought together scientists of various disciplines to make recommendations for the future direction of 
research in the various aspects of biological control, and to take advantage of the many new 
possibilities resulting from current biotechnological research. Many other recommendations for 
improving biological control research programs had been made previously by the cooperative USDA 
task force in 1978 (USDA 1978), and in papers delivered at the interdisciplinary USDA Symposium 
at Beltsville, MD, in 1980 (Papavizas 1981). The next interdisciplinary meeting was the National 
Interdisciplinary Biological Control Conference organized by CSRS and attended by many 
university, state agricultural experiment station, and ARS scientists, held in February 1983 at Las 
Vegas, NV. The Proceedings of this Conference contains many recommendations for future research 
areas and operational needs (Battenfield 1983). This was followed in March 1984 by the ARS 
Research Planning Conference on Biological Control organized by the NPS Biological Control 
Matrix Team and held at Laurel, MD. And finally, in July 1987, an ARS Workshop on Research 
Priorities in Biological Control was held at Beltsville, MD, during which the ARS National 
Biological Control Program (NBCP) was established. Proceedings of these two meetings are also 
replete with many recommendations on research and operational/coordination needs (USDA 1984a; 
King et al. 1988). Concern over the lack of effective coordination of biological control programs was 
a common theme in all of these meetings. The establishment of the NBCP was for the purpose of 
unifying, improving coordination of, and expanding research on, the use of biological agents for pest 
control within ARS, in full cooperation with other federal and state biological control organizations 
(King et al. 1988). 


Also in 1987, a Research Briefing Panel on Biological Control in Managed Ecosystems was 
established by the National Academy of Sciences Committee on Science, Engineering, and Public 
Policy (COSEPUP) which resulted in a published report (NAS 1987). Along with a number of 
recommendations for future biological control research, the Report contained a broad and 
controversial definition of biological control. (See Dietrick 1988; Garcia et al. 1988; Gabriel and 
Cook 1990, and the Introduction to this History.) 


In April 1988, biological control once more became represented on the ARS National Program Staff 
(NPS), with the appointment of R. S. Soper to the position of National Program Leader (NPL) for 
Biological Control (to which insect taxonomy was later added). One of Soper's first actions was the 
establishment of Biocontrol Working Groups (BWGs) consisting of Federal, State, and university 
biological control specialists in various disciplines to provide guidance to the ARS Biological 
Control "Matrix Team" in technical matters pertaining to the further development of the ARS 
National Biological Control Program. The BWGs established during 1989-90 were on Microbial 
Biological Control, Augmentation and Conservation Biological Control, Classical Biological 
Control, Ecology, and Natural Products. In addition, Soper began the development of a Plan for 
Biological Control for the 21st Century. And in 1990 an Interagency Biological Control Coordinating 
Committee (IBC*) was created, consisting of members from APHIS, ARS, CSRS, the Forest Service 
and Extension Service, with liaison representatives from other agencies, whose major function was to 
reestablish and maintain coordination among USDA agencies in matters regarding biological control. 
The NPL for Biological Control was once again vacated at the end of 1992 when Soper assumed the 
duties of Assistant Administrator for the Office of International Research Programs in ARS. In 
January 1993, the NPS biological control position vacated by Soper was filled by J. L. Krysan, as 
National Program Leader for Pest Management Systems. And in September, another major 
reorganization of the USDA was announced. One of the proposed actions was the consolidation of 
the ARS, CSRS, Extension Service, and National Agricultural Library into a new agency to be called 
the Agricultural Research and Education Service (ARES). The new USDA reorganization was 
approved by Congress in October 1994; however, ARS was retained as a separate agency. 


48 


The increased concerns from public and private sectors about environmental contamination and the 
need for increased use of nonchemical methods of pest control resulted in a recognition that 
regulations concerning these methods, particularly those regarding importation of exotic organisms 
for biological control purposes, needed to be examined and improved. Two major USDA workshops 
were held in 1991 on the subject of guidelines and regulations impacting biological control. These 
were organized in an attempt on the part of research scientists to provide some guidance for 
regulatory agencies involved (primarily APHIS and EPA) in assessing pertinent regulations to 
prevent the development of regulations that would have a severe, negative impact on biological 
control research and development. (Coulson and Soper 1989; Coulson et al. 1991; Charudattan and 
Browning 1992; Kauffman and Nechols 1992). Increasing public scrutiny of USDA biological 
control programs has led to considerable activity in APHIS, USDA's regulatory agency, regarding an 
overhaul of pertinent regulations and procedures dealing with these programs; see Chapter VI, and 
Epilogue. 


B. BIOLOGICAL CONTROL OF ARTHROPODS (INSECTS, MITES, AND TICKS) 
1. Arthropod Biological Control Agents 
a. Classical biological control (introduction of biological control agents). By J. R. Coulson 


Of all areas of ARS biological control research, classical biological control felt the effects of the 
1972 ARS reorganization the most severely, because, within ARS, this type of biological control 
involved sequential activities carried out by many people at widely distant locations. The previous 
centralized and effective coordination and direction of these activities, from the overseas biological 
control facilities to the biological control quarantine receiving facilities and other Insect 
Identification and Parasite Introduction Research Branch (IIPI) domestic facilities scattered in 
various regions and areas of the new ARS structure, was destroyed or fragmented. Subsequent 
attempts to reestablish such tight coordination have been largely unsuccessful. One immediate effect 
of the reorganization was the cessation of quarterly and annual reports of many of the old IIPI 
laboratories, in favor of new, less detailed reporting systems, with narrower distribution of reports 
than under IIPI and the Entomology Research Division. 


For a short period after the reorganization in 1972, the administrative offices of the now defunct IIPI, 
together with the Branch's Systematic Entomology Laboratory, became the Systematic Entomology 
and Beneficial Insect Introduction Laboratory (SEBIIL) of the Plant Protection Institute. The SEBIIL 
was one of nine newly created Institutes at the Beltsville Agricultural Research Center (BARC) at 
Beltsville, MD. 


In a memorandum to the ARS Administrator dated August 14, 1972, R. I. Sailer, former IIPI Branch 
Chief and at the time Laboratory Leader of SEBIIL, presented his ideas on "organizational 
requirements of an operationally effective biological control program" in ARS. In this memorandum, 
Sailer proposed the eventual development of a "National Institute of Biological Control and 
Beneficial Insect Research," and presented a list of its proposed responsibilities. These included line 
administrative authority for overseas biological control research and domestic quarantine receiving 
activities within each of the four ARS Regions, with the help of a Committee chaired by a National 
Program Staff (NPS) specialist for program supervision and budget development purposes. Such 
proposed centralized direction did not fit well into the new regionalized structure of ARS, and met 
with resistance. As a result, a second memorandum, prepared by A. A. Hanson, BARC Area 
Director, with Sailer's assistance, presenting revised ideas on the "proposed organization for 
coordination of ARS research on natural enemies of insects and weeds," was sent to the ARS 
Administrator September 22, 1972. These proposals included 1) establishment of an ARS Committee 
to Coordinate Research on Natural Enemies of Pests, 2) establishment of the Insect Identification and 


49 


Beneficial Insect Introduction Institute (IIBIII) at Beltsville (the Institute Chair to serve as Vice Chair 
of the Coordinating Committee), and 3) "maintaining close coordination between all units engaged in 
the introduction, colonization, evaluation and management of beneficial insects." Specific 
organizations and functions of the proposed Coordinating Committee and Institute were outlined in 
the memorandum. 


These proposals, and other proposals from the ARS Western Region, concerning overall coordination 
and national planning for research programs on natural enemies of insects and weeds were discussed 
by the ARS Board of Directors at various times. Though initially rejected, revised proposals 
eventually resulted in the approval in May 1973 of "A Plan for Coordination and Leadership of 
Biological Control Research in the Agricultural Research Service" and the creation of the Working 
Group on Natural Enemies of Insects, Weeds and Other Pests (WGNE) (see section A above, and the 
WGNE Charter in Appendix I.A). The IIBIII, with Sailer as Chair, was established at Beltsville in 
September 1972. 


Believing the lack of close centralized direction to be a fatal flaw in the ARS biological control 
program, Sailer retired in 1973 and moved to the University of Florida as a Distinguished Professor 
of Biological Control. A similar loss of a key USDA biological control specialist, C. P. Clausen to 
the University of California, occurred 20 years earlier under similar circumstances (weakening of 
strong centralized direction of USDA classical biological control research as a result of events 
culminating in the 1953 reorganization, see Chapter III). Sailer's views on the optimal organization of 
a strong classical biological control program later appeared in print (Sailer 1974, 1976b, 1981b; 
Beirne 1985). 


The new Institute (IIBIII) at Beltsville consisted of the Systematic Entomology Laboratory (SEL) and 
the newly created Beneficial Insect Introduction Laboratory (BIIL). At its inception, BIIL consisted 
of one entomologist (J. R. Coulson) and two clerical assistants, with responsibility for maintenance 
of the extensive files of IIPI, for providing information on classical biological control of arthropods 
and weeds as needed by scientists and administrators, and for otherwise assisting the Institute 
Chairman, Dr. Sailer, in working with the NPS to coordinate the ARS classical biological control 
programs. L. Knutson became Institute Chair following Sailer's retirement in 1973, and matters 
concerning coordination of ARS biological control programs were placed with HG new WGNE, with 
BIIL providing significant support. 


Line administrative authority for the overseas biological control laboratories was placed in the newly 
formed International Programs Division (IPD), and for the domestic quarantine facilities, line 
authority remained with the various areas and regions in which the facilities were located. Three 
Technical Advisors (TAs) were appointed in 1973 to assist IPD in managing the technical] details of 
the research programs of the three overseas biological control facilities, and to assist in providing 
some coordination of the overseas programs with quarantine and other domestic research facilities. 
The TAs were J. R. Coulson (of BIIL) for the European Parasite Laboratory (and later for the new 
Asian Parasite Laboratory), and L. A. Andres (ARS, Albany, CA) and C. J. DeLoach (ARS, Temple, 
TX) for the Biological Control of Weeds Laboratories in Italy and Argentina, respectively (see 
section C below). These roles were abolished in 1981 when line authority for the overseas facilities 
was placed in the newly created International Activities office, now the Office of International 
Research Programs (see section A above). 


In its information and coordination roles, BIIL also retained a special relationship with the biological 
control quarantine facilities and other domestic research facilities. A uniform system and set of forms 
for recording information on importation, domestic shipment, release and recolonization of beneficial 
invertebrates, which are used by most ARS facilities and some state and university facilities in the 

U.S., were developed by 1976 and improved in 1984, as a result of an extensive user survey (Coulson 


50 


1987a; 1992b). Biological control information documents were produced by BIIL, which contained 
rosters of U.S. and Canadian biological control workers, with brief description of their research 
areas, and other information of interest to biological control, the last of which was produced in 1985 
(Coulson and Hagan 1986). A number of historical surveys and evaluations of recent ARS classical 
biological control programs have been produced by BIIL (Coulson 1977, 1987b; Coulson in Doane 
and McManus 1981; Coulson et al. 1986). Also, BI[L was much involved in developing procedures 
or guidelines for importation of exotic beneficial organisms into the U.S. (Klingman and Coulson 
1982-83; Nickle et al. 1988; Coulson and Soper 1989; Coulson et al. 1991), and in assisting in 
biological control exchange programs, particularly with the USSR and PRC (Coulson 198 1a; 
Coulson et al. 1982). The information activities of BIIL, which received special funding in 1981, 
were formally recognized in 1982 by the establishment in BIIL of the ARS Biological Control 
Documentation Center, in which a number of computerized databases of importance to biological 
control were to be developed and maintained (see section A, and Epilogue, and Coulson 1987a, 1988, 
1992 b and c; Coulson et al. 1988; Knutson et al. 1990). 


In addition to these non-research functions, BIIL developed a research program, with the addition of 
research entomologists for biological control of insect pests (1973), for biological control of weeds 
(1974), for biosystematics of beneficial insects (1978), and for research on genetics of insects of 
importance to biological control (1984). Notes on BIIL's weed research program are included in 
section C below. Research on parasites and predators at BIIL (and after 1985 at BIL and IBL, see 
below) included studies on the gypsy moth, Mexican bean beetle, Colorado potato beetle, corn 
rootworms, asparagus beetles, and euonymus and other armored scales, and on biosystematics of 
Trichogramma parasites. (Schroder 1981, 1982; Nickle et al. 1984; Schroder and Athanas 1985; 
Hung and Huo 1985; Hung at al. 1985; Vincent and Goodpasture 1986; Drea and Carlson 1987, 
1988; Hendrickson and Drea 1988; Nalepa et al. 1993; Schroder et al. 1993.) 


In November 1985, BIIL was combined with the Bioenvironmental Bee Laboratory at Beltsville, and 
the combined laboratory became the Beneficial Insects Laboratory (BIL), headed by H. Shimanuki 
(1985-87) and J. J. Drea (1988-1990). At the same time, IIBIII became the Biosystematics and 
Beneficial Insects Institute (BBII), with three laboratories: SEL, BIL, and a new laboratory, the 
Systematic Botany, Mycology, and Nematology Laboratory (SBMNL), created from three taxonomic 
units in the Plant Protection Institute. One unfortunate result of this "mini-reorganization" was to 
begin the process of obscuring the identity of classical biological control introduction activities 
among the many research units at Beltsville. Also, support personnel for the ARS Biological Control 
Documentation Center were drastically reduced in the course of this reorganization, causing a 
corresponding reduction in BCDC's documentation activities. Then, in a larger reorganization at 
Beltsville in January 1988, BBII was abolished altogether, after 16 years of existence; SEL, BIL, and 
SBMNL became laboratories of a newly organized Plant Sciences Institute (PSI). The research and 
reduced documentation activities of BIL continued under the new organizational structure. 


There was a further reorganization in June 1990, in which the biological control personnel of BIL 
were incorporated with the insect pathologists of the Insect Pathology Laboratory (see later in this 
section) to form an Insect Biocontrol Laboratory (IBL) within the PSI, under the leadership of J. L. 
Vaughn. A Bee Research Laboratory was reconstituted, and BIL abolished. 


Before discussing the programs of other ARS units involved in classical biological control research 
from 1972-93, mention must be made of several other general events impacting upon this area of the 
ARS biological control program. The lack of a biological control specialist on the National Program 
Staff from 1972-76 and 1982-88, the development of National Research Programs (NRPs) and other 
research management systems from 1976-87, and the establishment, organization and activities of the 
ARS Working Group on Natural Enemies of Insects, Weeds and Other Pests (WGNE), have all been 
discussed in section A above. The establishment of Research Teams and Coordinating Subgroups to 


51 


assist in the coordination of research programs crossing ARS area and regional boundaries was one 
of the functions of the WGNE. No Research Teams and only one Coordinating Subgroup were 
actually established by the WGNE. 


A Coordinating Subgroup on Biological Control of Lygus spp. and Other Plant Bug Pests in the U.S. 
was established in June 1980, its first of a series of meetings being held in July 1980. Subgroup 
members included representatives from five domestic ARS laboratories, the European Parasite 
Laboratory, Texas A & M University locations at College Station and Dallas, and eventually the 
University of Oregon and two research stations in Canada, all locations conducting biological control 
or taxonomic research on plant bugs or their parasites. The Subgroup’s objectives were: 1) to provide 
joint planning for exploration for and quarantine receipt of natural enemies; 2) to expedite research 
on testing and propagation of the natural enemies and to facilitate their dissemination to federal and 
state agencies for laboratory studies and field releases; 3) to provide for an adequate exchange of 
information among all involved locations; and 4) to coordinate the evaluation of field releases and 
the reporting of results of establishment of natural enemies and of their effectiveness. The Subgroup 
produced a bibliography (Graham et al. 1984) and a publication of their activities (Hedlund and 
Graham 1987), and met biennially on an ad-hoc basis through 1991. 


The WGNE was instrumental in creating, for a short period during the late 1970s, a foreign 
exploration fund consisting of $40,000 annually from the ARS Administrator's funds. Proposals for 
explorations were reviewed and prioritized by the WGNE. Beginning in 1989, ARS funds for foreign 
explorations, mostly involving specific pests, again became available, and ARS began to solicit 
proposals annually from both federal and state scientists for explorations. These proposals were 
evaluated and ranked by the ARS Biocontrol Working Group on Classical Biological Control, the 
ARS Biological Control Matrix Team, and the Interagency Biological Control Coordinating 
Committee; see section A. 


The establishment, organization, and activities of the interdepartmental USDA Work Group on 
Biological Pest Control Agents (WGBCA) was also discussed in section A above, and its charter is 
presented in Appendix I.B. One of the several interdepartmental subcommittees established by the 
WGBCA was the Subgroup on Introduction of Biological Control Agents (SIBCA) (Coulson and 
Soper 1989). SIBCA was established in November 1976 with members from ARS, APHIS, CSRS, 
and FS, with the responsibility of responding to requests from APHIS concerning the propriety of 
certain intended introductions of entomophagous insects and nematodes, insect pathogens, 
antagonists of plant pathogens and nematodes, or other biological control agents, except those 
intended for control of weeds (which were evaluated by another interagency group; see Chapter III, 
section B, above). Only "controversial" cases involving permit applications for introduction of exotic 
biological control agents were submitted for SIBCA review by APHIS. SIBCA became defunct with 
the WGBCA in 1981. 


Also discussed in section A above, are the various task forces, conferences, and workshops from 
1978-87 in which concerns were expressed and recommendations made concerning the need for 
strengthening biological control research, including improvement in the effective coordination of 
such programs in the United States. For the most part, it was classical biological control that was 
perceived to be in most need of strengthening and improved coordination. This area of research in the 
U.S. had long been conducted largely by the USDA, the University of California, and the Hawaiian 
Department of Agriculture, all of which maintained biological control quarantine facilities, and 
adequate program coordination was relatively simple. As mentioned previously, the classical 
biological control program of the University of California operated under a Memorandum of 
Agreement between the State of California, the University and USDA (Appendix I.C). 


2 


In the early 1970s, other university and state agencies began to develop classical biological control 
programs. These new programs included quarantine receiving facilities, beginning with the approval 
of that of the Virginia Polytechnic Institute and State University (VPI) in 1970, and the Florida 
Department of Agriculture and Consumer Services facility in 1973. The latter facility operated 
cooperatively with the University of Florida and USDA-ARS at Gainesville. Quarantine facilities and 
importation programs were established by Texas A & M University at College Station in 1981, by 
the North Carolina Department of Agriculture at Raleigh in 1984, and by Montana State University 
at Bozeman in 1988. Other state/university and federal quarantine facilities have since been opened, 
or are under construction or planned (Coulson et al. 1991). In order to operate, all quarantine 
facilities must be initially (and periodically thereafter) inspected and approved by APHIS-PPQ. ARS 
draft guidelines for importation of exotic natural enemies were prepared, which included guidelines 
for quarantine facility operation (Coulson et al., 1991), and contained provisions requiring the 
establishment of MOA's for all federal/state/university quarantine facilities similar to that for the 
University of California facilities; but no such MOA's were ever established for any of the new 
facilities. The proliferation of biological control quarantine facilities and importation programs has 
made information exchange between them, documentation of importation and release of exotic 
organisms, and coordination of classical biological control programs much more difficult. 


In a 1979 report by the Office of Technology Assessment of the U.S. Congress on Pest Management 
Strategies in Crop Protection (OTA 1979), it was recommended that "the classical biological 
approach on insect and mites, especially exotic species, is one to be stressed," and increased funding 
for this purpose was recommended. But the report also recommended a reorganization of biological 
control efforts, including modification of the "present Federal horizontal structure" to a "centrally 
organized, vertically structured unit," and the formation of a national biological contro] planning 
body with more even representation among ARS, APHIS, FS, CSRS, the Extension Service (ES), and 
the states, than existed on the ARS-WGNE. Also in 1979, a proposal for establishing a National 
Program for Biological Control was presented at the annual Entomological Society of America 
meeting that year (Gilstrap and Cate 1979). The authors noted their reason for devising the plan was 
a perception that biological control was struggling because of inadequate organization, support, and 
leadership. The plan, which was preliminary and never published, identified needs for more support 
for taxonomic research and identification services, improved guidelines and support for quarantine 
facilities, and functional regional and national records systems. Parts of the recommendations of the 
1978 USDA report (USDA 1978) and of the 1979 OTA report (OTA 1979) were addressed by the 
proposal (R. L. Ridgway in litt. 1979). Recommendations for improving communication, 
coordination, and cooperation between the many USDA and state/university biological control 
programs were included among the many recommendations of the 1983, 1984, and 1987 conferences 
(Battenfield 1983; USDA 1984a; King et al. 1988). 


The development of the APHIS-PPQ biological control implementation program from its initiation in 
ARS with the cereal leaf beetle (CLB) program (see Chapter III, section A) is discussed in Chapter 
VI. The need for an agency that would handle the large-scale distribution of established effective 
natural enemies was recognized during the ARS alfalfa weevil program. USDA research scientists at 
the ARS quarantine facility in New Jersey (later Delaware) were heavily involved in dissemination 
of established alfalfa weevil parasites. The biological control program of the New Jersey Department 
of Agriculture joined in this effort and combined efforts had soon established the parasites 
throughout New Jersey. But ARS research scientists still were involved in distributing the parasites 
to other states, at the expense of research time. The highly successful CLB parasite distribution 
program of the APHIS-PPQ laboratory in Niles, MI, gave evidence as to the benefits of such an 
implementation program. Therefore, ARS scientists at Newark, DE, and Beltsville, MD, were highly 
supportive of the development of the PPQ biological control implementation program (Coulson 
1976; Sailer 1976b), which was initiated in 1980. The program has been highly successful, and a 
1985 team reviewing the program recommended that APHIS-PPQ "continue as a leader in biological 


515) 


control by assisting research and implementing action projects." As recommended by the review 
team, a biological control specialist was added to APHIS-PPQ to assist in the development and 
coordination of the program. In 1988, the APHIS program embarked on a new initiative which was 
designed to expedite natural enemy importation, quarantine screening, and mass rearing and release 
efforts. The APHIS initiatives in foreign explorations and collections, importation, and quarantine 
screening seemingly conflicted with ARS efforts in these areas. Attempts were renewed in 1989 to 
establish a joint APHIS-ARS biological control committee to coordinate efforts in these areas. As 
noted in section A above, these efforts culminated in formation of the Interagency Biological Control 
Coordinating Committee (IBC’*) in the USDA. 


During 1973-93, ARS biological control research continued at the three overseas laboratories, and at 
a fourth laboratory, the Asian Parasite Laboratory, which was reestablished in 1975. Projects at the 
laboratories in Italy and in Argentina continued to be almost exclusively devoted to biological 
control of weeds (see section C). However, at the Biological Control of Weeds Laboratory at 
Hurlingham, Argentina, there were also projects on pathogens and other natural enemies of 
grasshoppers, pickleworm, and on dung beetles for control of dung-breeding flies, for the ARS 
laboratories at Bozeman, MT, Charleston, SC, and College Station, TX, respectively. In addition, the 
Argentine laboratory provided strong logistical and other support for visiting U.S. explorers seeking 
natural enemies of insect pests in South America of potential use in U.S. biological control programs; 
such explorations included several groups of university and ARS scientists studying natural enemies 
of soybean insects (velvetbean caterpillar, soybean looper, etc.) in the early 1980s (see Jones et al. 
1983; Boethel and Orr 1990), and ARS scientists studying enemies of corn rootworms (Diabrotica), 
in 1988 and 1991. However, by the end of 1993, the mission of the Argentine laboratory, renamed 
the South American Biological Control Laboratory, was changed drastically to concentrate almost 
exclusively on insect target pests, including the Heliothis/Helicoverpa moth complex, Diabrotica 
beetles, sugarcane borer, pickleworm, and fire ant, with only one target weed remaining (H. A. 
Cordo, pers. commun., 1993). 


Research at the European Parasite Laboratory (EPL) in France from 1973-91, and later at the 
consolidated European Biological Control Laboratory (EBCL) (see below) in 1991-93, concerned 
natural enemies of the following insect pests: alfalfa blotch leafminer (1973-80); lygus and other 
plant bugs (1973-88); gypsy moth (1973-92); alfalfa snout beetle (1973-74); grasshoppers (1973-77); 
elm leaf beetle (1973, 1981-82); European corn borer (1974); Eurasian pine adelgid, for Hawaii 
(1975-77); Sitona weevils (1975-79, 1982-84); greenbug and other grain aphids, for Oklahoma, 
Texas, Chile, and Brazil (1975-82); alfalfa weevil, for APHIS, California, and Canada (1976, 
1979-82); bark beetles (1977-81); birch leafminer (1979-82); green peach aphid (1979); horn fly and 
other dung-breeding flies (1979-91); anthomyiid maggots (1979-80); euonymus scale (1981); pear 
psylla (1981-83); asparagus beetles and asparagus aphid (1982-87); noctuid pests (Heliothis, 
Autographa, and Spodoptera) (1982-86); Empoasca leafhoppers (1984-86); nitidulid sap beetles 
(1985); cockroaches (1986-88); southern green stink bug (1986-87); "apple ermine moth" (1988-92); 
Russian wheat aphid (1988-92); codling moth (1990-92); and sweetpotato whitefly (1991-93). 
Explorations and collections were made by EPL and EBCL personnel throughout Europe, and in 
North Africa, Iran, Turkey, the USSR and countries of the later Commonwealth of Independent 
States, China and Japan. EPL and EBCL Directors during this period were J. J. Drea (1969-80), R. C. 
Hedlund (1980-81), B. D. Perkins (1981-86), R. F. Moore (1986-89), and L. Knutson (1990-93). 
(Drea 1981; Hoyer 1981, 1986; Hérard 1985, 1986; Blanchot 1992; Lacey et al. 1993; Gruber et al. 
1994; and other references listed below under significant accomplishments of the period.) 


Beginning in the mid-1960s, considerable effort was expended by ARS to consolidate the two ARS 
European biological control laboratories, at that time both in unsuitable rented facilities. In the 
1970s, plans were made for constructing a modern ARS research facility at a location near the 
biological control laboratory of the French Institut Nationale de Recherche Agronomique (INRA) 


54 


near Antibes in southern France. These efforts failed in 1980, and in late 1983, the EPL moved into 
purchased facilities at Béhoust, about 40 kilometers west of Paris. (The Rome laboratory moved into 
better rented facilities in 1981.) Efforts to consolidate the two laboratories resumed in 1988, and by 
the end of that year, consideration was being made for the location of a consolidated laboratory at 
Montpellier in southern France. The two laboratories were finally united in temporary facilities at 
Montpellier in September 1991, as the European Biological Control Laboratory (EBCL), under the 
leadership of L. Knutson. Unfortunately, accompanying the consolidation was a loss of several long 
term employees of both laboratories. Construction of facilities for the EBCL was scheduled to begin 
in 1998. One-man substations of the EBCL were retained in Italy and Greece, and their pipers 
broadened to included research on insect pests as well as weeds. 


In 1981, an insect pathology research program was initiated at the EPL under cooperative 
agreements, and was formalized at the 1983 EPL program review (see below); this became an official 
part of the EBCL program in 1991. Pathogens from the various EPL/EBCL target pests under study 
have been isolated at EPL/EBCL and many have been shipped to the ARS Insect Pathology Research 
Unit at Ithaca, NY, and the Insect Pathology Laboratory (Insect Biocontrol Laboratory since 1990) at 
Beltsville, MD, from 1981 to the present. See Appendix II for more details of the European 
pathology program. 


In October 1983, the programs of the EPL and the Rome laboratory underwent a high level review by 
ARS and many other scientists and administrators, the first major review ever held for the ARS 
overseas laboratories. Among many recommended changes in administration and research resulting 
from the review, that can be noted in the proceedings of the review, was a controversial 
recommendation that EPL markedly increase the percentage of publishable "basic research" at the 
expense of "service work" (i.e., the search for, collection, and shipment of natural enemies); these 
services, which are essential to a successful biological control program, are often viewed as 
non-research activities by administrators and peer reviewers, and promotions for overseas personnel 
have lagged behind those of their domestic colleagues. In recent years, a better balance between 
research and service has been sought in the European program. 


In May 1975, an ARS Asian Parasite Laboratory (APL) was reestablished by P. W. Schaefer, with 
the help of special funds made available for ARS biological control research on the gypsy moth 
(Coulson 1981b; Schaefer 1981; Pemberton et al. 1993). (See Chapters I and II for information 
regarding the earlier Asian Parasite Laboratory.) The reestablished APL was first located at Sapporo, 
Hokkaido, northern Japan, which was near known populations of the gypsy moth, the major target 
pest for the laboratory. In 1982, the APL was relocated to Seoul, South Korea, as a result of the need 
to conduct research on additional target pests. Research at the APL in Japan and South Korea 
concerned natural enemies primarily of the gypsy moth (1975-93), but also of the following 
additional insect pests: larch casebearer (1976); "oriental chestnut gall wasp" (1977-79, 1984-89); 
Fiorinia scales (1977); Japanese beetle (1978, 1982, 1987-88); "Asian corn borer" (1978-79, 
1985-87); epilachnine beetles (1979-88); pear psylla (1979-80); red pine scale (1979-80, 1983-84); 
southern green stink bug (1979-85); green peach aphid (1979); euonymus and other armored scales 
(1982-86); imported cabbageworm (1988); and "apple ermine moth" (1988-91). Studies by APL 
personnel were also conducted in China, on the "apple ermine moth" (1990-91) and "Asian gypsy 
moth" (1991-92), and in Russian Far East, on the latter in 1992. Research on biological control of 
weeds was also begun by APL personnel, in 1991 (see section C). ARS scientists in charge of the 
new APL were P. W. Schaefer (1975-79), R. W. Carlson (1980-85), D. K. Reed (1985-88), and R. W. 
Pemberton (1989-93). (Schaefer 1981; Schaefer and Ikebe 1982; Drea and Carlson 1987, 1988; 
Schaefer et al. 1988; Pemberton et al. 1993.) An administrative decision was made by ARS in 1993 
to close this laboratory at the end of the fiscal year, and the long history of the USDA Asian Parasite 
Laboratory, which first opened in the 1920s, ceased. 


on) 


In the past, foreign explorations could generally be carried out over many parts of the world from 
ARS overseas laboratories. Research on exotic natural enemies in some areas of the world could also 
be carried out under the SFC or PL-480 program, which has been continued under OICD 
administration. There have been three large geographical areas of the world where such explorations 
and research have been more difficult or impossible: the area of the former Union of Soviet Socialist 
Republics (USSR), the People's Republic of China (PRC), and Australia and the South Pacific. As a 
result of a 1972 US-USSR agreement in the area of environmental protection, U.S. and Soviet 
specialists began exchanging biological control agents in 1972, and there were several ARS 
exploration trips in the USSR under this agreement (Coulson 1981a). From the U.S. viewpoint, 
results were somewhat disappointing. An agricultural agreement was also signed with the PRC, in 
1978, and exchanges of biological control agents and personnel were begun in 1979 between Chinese 
and American specialists (Coulson et al. 1982; Knutson and Gordon 1982). These, too, were largely 
unsatisfactory, though some materials were exchanged. Negotiations conducted by ARS (R. S. Soper 
and others) and the Chinese Academy of Agricultural Sciences in 1988 have resulted in the 
establishment of a Sino-American Collaborative Biological Control Laboratory in Beijing, PRC, in 
November 1988, greatly improving the situation in regard to obtaining biological control agents in 
the PRC. By the end of 1988, similar agreements with the Zoological Institute of the USSR Academy 
of Science in Leningrad, and the All-Union Institute for Biological Methods of Plant Protection in 
Kishinev, Moldavian SSR, also greatly improved cooperative US-USSR efforts in biological control. 
The breakup of the Soviet Union in 1991 caused problems with these arrangements, and efforts are 
being made to reestablish cooperative linkages. And finally, in 1989, an ARS laboratory was 
established in Australia, primarily for study of natural enemies of aquatic and wetland weeds, but 
with potential to expand into other areas of biological control; see section C.1 below. 


Special relationships were maintained between the principal domestic ARS quarantine facility for 
parasites and predators at Newark, DE, (having moved from Moorestown, NJ, in 1973; see also Ertle 
and Day 1978) and the European and Asian Parasite Laboratories. Similar relationships were 
maintained by the ARS quarantine facilities for natural enemies of weeds at Albany, CA, and at 
Temple, TX, with the weeds laboratories at Rome, Italy, and Hurlingham, Argentina, respectively; 
see section C, below. In addition to a large quarantine clearance service for imported parasites and 
predators destined for many state and other federal biological control programs, the Beneficial 
Insects Research Laboratory (BIRL) at Newark, DE, maintained a research program during 1973-93, 
based primarily on material received from the programs of the EPL/EBCL and APL. Imported 
natural enemies were released, and their establishment, dispersal, and impact evaluated. These 
included natural enemies of: alfalfa weevil (1973-88); gypsy moth (1973-93); cereal leaf beetle 
(1973-77); alfalfa blotch leafminer (1973-82); pea aphid and other aphids (1973-88); lygus and other 
plant bugs (1976-93); European corn borer (1974-77); birch leafminer (1974, 1978-88); Sitona 
weevils (1975-86); asparagus aphid (1975); Mexican bean beetle (1975-76, 1979-88); spider mites in 
greenhouses (1980, 1985); Colorado potato beetle (1981-84); larch casebearer (1980-86, 1991-92); 
European wheat stem sawfly (1982-83); asparagus beetles (1983-87); potato leafhopper (1983-87); 
and euonymus and other armored scales (1986-88). (See pertinent references cited below under 
significant accomplishments of the period.) BIRL's alfalfa weevil program and the support given by 
BIRL scientists in the development of the APHIS-PPQ biological control implementation program, 
have been discussed in section A. The APHIS program has relieved BIRL scientists of the large task 
of disseminating established, effective alfalfa weevil parasites to new areas. Research Leaders at 
BIRL (renamed BIIR, Beneficial Insects Introduction Research, in 1989) during this period have 
been W. H. Day (1971-78), R. J. Dysart (1978-87), and R. W. Fuester (1987-present). 


The research program of the Biological Control of Insects Research Laboratory (BCIRL) at 
Columbia, MO, during 1973-93 largely concerned parasite/predator augmentation and insect 
pathology (see sections B.1.b and B.3 for more information and list of research leaders for this 
Laboratory). However, BCIRL personnel (principally B. Puttler) were involved in release and 


56 


evaluation of both exotic insect parasites and predators, and exotic weed-feeding insects. Puttler also 
conducted three foreign explorations during this period that resulted in the discovery and 
introduction of two new and important parasites of insect pests. One of these, Edovum puttleri, is a 
species currently being studied at many locations for use in Colorado potato beetle parasite 
augmentation programs, and the other, Euplectrus puttleri, has been established in Florida as an 
effective parasite of the velvetbean caterpillar. (Waddill and Puttler 1980; Puttler and Long 1983; 
Puttler et al. 1980; Schroder et al. 1985.) 


The ARS Stoneville Research Quarantine Facility (SRQF) at Stoneville, MS, which opened in 1973, 
had been planned and designed by IIPI as part of a special program on potential biological control of 
narcotic plants. The facility was also designed to serve as the major quarantine facility for classical 
biological control of weeds research in the eastern U.S., comparable to the facility at Albany, CA, for 
the western U.S. After the reorganization, an entomologist was stationed at the Southern Weed 
Science Laboratory (SWSL) at Stoneville for this purpose until the mid-1980's, but the classical 
program waned at the SWSL in favor of augmentative and pathology programs (see section C 
below). However, the WGNE recommended that the SRQF also serve as a major quarantine facility 
for insect parasites and predators for the southeastern U.S., to help lighten the heavy service load of 
the ARS quarantine facility at Newark, DE. Classical biological control of insects research began at 
the SRQF and the Bioenvironmental Insect Control Laboratory (Southern Field Crop Insect 
Management Laboratory, SFCIML, 1981-89, Southern Insect Management Laboratory, SIML, since 
1989) at Stoneville in 1978; research leaders of this unit have been E. G. King, 1981-88, and D. D. 
Hardee, 1988-present. Projects there have included research on natural enemies of graminaceous 
stemborers, Heliothis (s. lat.), plant bugs, and other insect pests of cotton and soybean, and the 
southern green stink bug. During the early 1980s, the SRQF served as quarantine facility for the 
many explorations by state and federal entomologists involved in the EPA-supported Soybean 
Subproject of the Consortium for Integrated Pest Management. During this period, SRQF also served 
as the quarantine receiving facility for parasites of lygus bugs from Africa destined for release in 
southwestern U.S. The facility still serves as a quarantine receiving center, but on a reduced basis, 
briefly (1992) responsible for quarantine receipt of imported parasites of the sweetpotato whitefly. 
(Bailey and Kreasky 1978; Jones et al. 1983, 1985; Coulson 1987b; Schuster 1987; Snodgrass and 
Ertle 1987; Powell 1989; Parencia and Martin 1990; Tillman 1993.) 


IIPI had also opened another station, at Gainesville, FL, just prior to the 1972 reorganization. The 
purpose of the station, located at the quarantine facilities of the Florida Biological Control 
Laboratory (FBCL) (Denmark 1978), was research on natural enemies of aquatic weeds, and research 
in this area has continued there (see section IC). During a short period in the 1970s, ARS personnel 
there (N. R. Spencer in charge) also began to engage in receipt and quarantine clearance of 
introduced insect parasites and predators, mostly scale insect parasites. The ARS station at 
Gainesville is now a satellite of the ARS Aquatic Plant Management Laboratory at Fort Lauderdale, 
FLy 


Other ARS facilities, not originally IIPI locations, have also been involved in research involving 
introduced natural enemies of insect pests during 1973-93. These include work on lygus bug 
parasites at the ARS Biological Control of Insects Laboratory (later named the Honey Bee Research 
unit) at Tucson, AZ, and the SFCIML at Stoneville, MS (Hedlund and Graham 1987); work on pear 
psylla predators and parasites (Fye 1981; Unruh et al. 1995), and "apple ermine moth" parasites 
(Unruh et al. 1993; Unruh 1995), at the Yakima Agricultural Research Laboratory at Yakima, WA; 
work on various citrus pests at ARS locations at Weslaco, TX, and Riverside, CA (the latter research 
location being abolished in 1987); research on introduced natural enemies of pecan and other 
arboreal aphids at the Southeastern Fruit and Tree Nut Research Laboratory at Byron, GA (Tedders 
and Schaefer 1994); studies of pathogens and nematodes attacking corn rootworms collected in 
Argentina at the Northern Grain Insects Research Laboratory at Brookings, SD; and, most recently, 


57 


work on imported parasites and predators of the newly introduced Russian wheat aphid at ARS 
facilities at Stillwater, OK, and Brookings, SD. The laboratories in Arizona, Mississpppi, 
Washington, Texas, and South Dakota have also been much involved in augmentation research; see 
section B.1.b below. Research on an imported parasite of rangeland grasshopper eggs was conducted 
under a cooperative ARS-APHIS program by R. J. Dysart at the ARS Northern Plains Soil and Water 
Management Research Center, Sidney, MT (Dysart 1991, 1992). These studies generated much 
controversy in the scientific press concerning the release of exotic natural enemies against native 
pests; see Lockwood 1993 a and b; Carruthers and Onsager 1993, and also section B.3 below. This 
research followed up much earlier research on grasshopper natural enemies conducted at the ARS 
Rangeland Insect Laboratory at Bozeman, MT, utilizing parasites received from the ARS European 
Parasite Laboratory (see Chapter III, section A.1.a). A compendium of known grasshopper parasites 
and predators in North America was published as an outgrowth of those early studies (Rees 1973). 


Following the lead of the Hawaiian Department of Agriculture and University of California 
biological control programs, ARS began intensified research during this period on classical 
biological control of insect pests of livestock. The first importations of exotic dung beetles for 
control of dung-breeding flies were made in 1972 by personnel of the Veterinary Toxicology and 
Entomology Research Laboratory (name changed to Food Animal Protection Research Laboratory in 
1991) at College Station, TX (Fincher 1986; Coulson and Soper 1989). Importations of several 
species of exotic histerid and staphylinid predators of dung-breeding flies were begun in 1985 at that 
Laboratory (G. T. Fincher, personal communication, 1992); the ARS importation of the staphylinid 
predator Aleochara tristis in the 1960s is noted in Chapter III. Importations of parasites of 
dung-breeding flies began in the early 1980s at the Insects Affecting Man and Animals Research 
Laboratory (name changed to Medical and Veterinary Entomology Research Laboratory in 1991) at 
Gainesville, FL, utilizing the FBCL quarantine facilities (Hoyer 1981, 1986; Morgan 1986). The 
Gainesville and other ARS facilities are also involved in considerable research on augmentation of 
natural enemies of livestock pests and on pathogens of insects affecting both livestock and man (see 
sections B.1.b. and 3, below). 


Also during this period of classical biological control, apparently the first introductions of exotic 
insect-parasitic nematodes in the U.S. were made by ARS (Coulson 1981c; and section B.2 below), 
and, as noted above and in section B.3 below, ARS began importing exotic insect pathogens. By 
1988, forms were developed by the ARS Biological Control Documentation Center for documenting 
the importation and release of exotic insect and weed pathogens and microbial antagonists of plant 
pathogens and nematodes (Coulson 1992b). 


Significant accomplishments resulting from the USDA-ARS classical biological control program 
during 1973-93 include the control of the alfalfa blotch leafminer in the northeastern U.S. and of the 


Eurasian pine adelgid in Hawaii, and of grain aphids in some parts of South America, and the 
establishment of natural enemies of the gypsy moth, plant bugs, euonymus scale, birch leafminer, and 
arboreal aphids. Numerous exotic parasites, predators, and pathogens of the gypsy moth (see section 
A.3) and, since 1987, of the Russian wheat aphid and sweetpotato whitefly, have been collected and 
made available to many federal, state, and university research workers in the U.S. for study and 
release against these pests (Lacey et al. 1994). In addition, ARS research resulted in the importation 
of two exotic parasites that have been utilized in augmentation programs for control of the Mexican 
bean beetle and Colorado potato beetle during this period. 


The alfalfa blotch leafminer was first found in the U.S. in 1968 and quickly spread extensively in 
northeastern U.S. and eastern Canada. Not only did it cause considerable loss in alfalfa yield, but 
insecticidal treatments used by farmers to combat it threatened to upset the successful alfalfa weevil 
biological control program by decimating the introduced alfalfa weevil parasites. Research conducted 
both at the European Parasite Laboratory (1973-79) and the ARS Beneficial Insects Research 


58 


Laboratory (BIRL) in New Jersey and Delaware (1970-82), resulted in the discovery and importation 
of 14 European leafminer parasites, three of which have become established in the U.S. These three 
parasites caused a remarkable degree of control of the pest by 1981 in Delaware, and rapidly 
dispersed throughout the range of the pest in northeastern U.S. and Canada, with the result that no 
further insecticidal treatments are required. An annual savings of about $13,200,000 ($17,200,000 in 
1993 dollars) due to yield losses no longer encountered has been estimated; this does not take into 
account the cost of insecticides no longer applied. (Drea et al. 1982; Hendrickson and Plummer 1983; 
Drea and Hendrickson 1986; DeBach and Rosen 1991; and Chapter III, Table 1 above.) 


The Eurasian pine adelgid was first found in Hawaii in 1970, and rapidly spread through the islands 
causing severe damage to pines. Chemical eradication attempts failed, and requests for natural 
enemies were made of the ARS European Parasite Laboratory. EPL personnel collected in France 
and shipped to Hawaii a predator of the adelgid, the establishment and spread of which has resulted 
in effective control of the pest in Hawaii. (Culliney et al. 1988.) 


In connection with the greenbug program at the EPL, shipments of aphid parasites were sent to Chile, 
Brazil, and Argentina, to help combat the ravages of several species of grain aphids in those 
countries. Complete control of two of the aphids (Metopolophium dirhodum and Sitobion avenae) by 
the introduced parasites has been claimed in some areas of South America. (Rojas 1980; Zufiiga 
1985; Gruber at al. 1994.) Releases of the European parasites in Oklahoma and Texas apparently 
were unsuccessful. 


Explorations for gypsy moth parasites were conducted by personnel of both the European and the 
Asian Parasite Laboratories, and release and evaluation studies were conducted by personnel of 
BIRL in Delaware. BIRL was also much involved in quarantine clearance of imported gypsy moth 
natural enemies for study and release by the Forest Service and state biological control programs in 
New Jersey, Pennsylvania, Virginia, Maryland, West Virginia, and North Carolina. An APHIS 
Gypsy Moth Parasite Distribution Program was developed to help distribute the introduced parasites 
being cultured by the New Jersey Department of Agriculture. Only one species (Coccygomimus 
disparis) of the many introduced parasites has been successfully established so far from this 
program; it is too early to note whether the parasite will have an impact on gypsy moth populations. 
(Drea 1978; Coulson 1981 b and d; Fuester et al. 1981, 1988; Schaefer 1981; and other sections in 
Doane and McManus 1981; Schaefer et al. 1984, 1988, 1989; Coulson et al. 1986.) 


Extensive research on natural enemies of lygus bugs and other plant bug pests has been conducted by 
personnel of the EPL and BIRL, and by some other ARS laboratories, during this period. Several 
European parasites have been introduced, and two species are firmly established in northeastern U.S. 
In 1987-88, one, Peristenus digoneutis, increased field parasitism of the tarnished plant bug to three 
times the previous rate by native parasites; the other, P. conradi, has raised field parasitism of the 
alfalfa plant bug by four times. Potential savings if adequate control of these two pests is eventually 
obtained ranges from $60 to $130 million per year (W. H. Day, personal communication, 1993). 
(Coulson 1987b; Day 1987; Hedlund 1987; Day et al. 1990, 1992.) 


Beginning in 1980, research on the parasites and predators of the euonymus scale was conducted at 
the Asian Parasite Laboratory, and at BIRL in Delaware, and the Beneficial Insects Laboratory at 
Beltsville, MD. Several parasites and two predators, Chilocorus kuwanae and Cybocephalus sp. 
prob. nipponicus, were introduced, and the two beetle predators have become established. Results so 
far have been rather spectacular, the beetles being responsible for complete eradication of the scale in 
release sites in several States. A large program for the wide-scale dissemination of the established 
predators is being conducted by ARS, which is slated to become part of the APHIS-PPQ 
implementation program in the near future. (Drea and Carlson, 1987, 1988; Hendrickson and Drea 
1988; Nalepa et al. 1993.) 


59 


Another pest of ornamentals, the birch leafminer, was first found in the U.S. in 1923, and has since 
dispersed throughout the northeastern U.S. and eastern Canada. European parasites were obtained 
from the Commonwealth Institute of Biological Control (CIBC) station in Europe and the ARS EPL 
and released by ARS personnel of the Delaware laboratory in Delaware, Maryland, Pennsylvania, 
and New Jersey in 1977-82, and two parasites became established (Fuester et al. 1984). The parasites 
are dispersing but it is still too early to assess their effect on birch leafminer populations. 


An Asian coccinellid predator of arboreal aphids, Harmonia axyridis, was first introduced in 1978 
for use against various pest aphid species and pear psylla. With releases made in Connecticut, 
District of Columbia, Delaware, Georgia, Louisiana, Maryland, Maine, Mississippi, Ohio, 
Pennsylvania, Washington, and in Canada during subsequent years, establishment was first 
confirmed in Louisiana in 1988 (Chapin and Brou 1991). This recovery was quite removed from 
intentional release sites and therefore may have resulted from accidental introduction. Nevertheless, 
in recent years its presence has been confirmed in Louisiana, Alabama, Mississippi, Georgia, North 
Carolina, Virginia and West Virginia, and most recently Washington. Its impact on arboreal aphid 
pests remains uncertain, but in some locations it is reportedly abundant. (P. W. Schaefer, BIRL, 
personal communication; Tedders and Schaefer 1994; see also Day et al. 1994, for comments on 
possible origin.) 


Earlier research by personnel of the ARS laboratory in Moorestown, NJ (now BIIR, Newark, DE), on 
a parasite of epilachnine beetles imported from India, Pediobius foveolatus, for control of the 
Mexican bean beetle (MBB), established the fact that the species could not overwinter in the U.S. 
But because the parasite otherwise proved to be an effective parasite of MBB larvae, research at the 
University of Maryland, funded by ARS, showed that the parasite could be used effectively in an 
augmentation program. This concept was then carried further in a large-scale APHIS-PPQ 
demonstration project involving several mid-Atlantic states (see Chapter VI), and the parasite is still 
being used for Mexican bean beetle control by the New Jersey and Maryland Departments of 
Agriculture. Savings are estimated to be $1,000,000 per year in New Jersey, and $3.26/acre of fields 
treated with the parasite in Maryland (W. H. Day, personal communication, 1993). (Stevens et al. 
1975; Reichelderfer 1979; Schroder 1981.) Other Asian and South American parasites and predators 
of the Mexican bean beetle have been under study at BIIR in more recent years. 


Explorations in South America in 1980 by BCIRL reported above, resulted in the discovery and 
importation of Edovum puttleri, which, though originally from eggs of a related beetle, successfully 
attacks eggs of the Colorado potato beetle (CPB). ARS research showed that this species, too, could 
not successfully overwinter in the U.S., and the species has become the subject of several 
augmentation programs for control of the CPB in eggplant, tomatoes, and potatoes. It has been shown 
to be an effective and economic control agent for the beetle in eggplant. (Schroder and Athanas 1985, 
1989; Schroder et al. 1985; Lashomb et al. 1987, 1988.) 


b. Augmentation and conservation of parasites and predators. By D. A. Nordlund and E. G. King 


Augmentation and conservation biological control received increased attention during the 1973-1993 
period as environmental concerns, regulation of pesticides, and resistance to insecticides increased. 
Knipling (1979, 1992) even suggested, based on theoretical simulation models, that augmentation of 
host specific parasites and predators could provide a solution to some of the world's major insect pest 
problems. A number of reviews pertinent to augmentation and conservation were published during 
this period including: Chapman 1974; Rabb et al. 1976; Bay et al. 1976; Ridgway and Vinson 1977; 
Ables and Ridgway 1981; Stinner 1977; Nordlund et al. 1981; Rutz and Patterson 1990; Anderson 
and Leppla 1992; and Williams and Leppla 1992. Also pertinent is the widespread adoption of 
integrated pest management (IPM) programs during this period (Hoy and Herzog 1985). Though 


60 


many IPM programs were in practice basically pesticide management programs, they did contribute 
significantly to conservation. 


Research by ARS scientists related to augmentation of entomophagous insects also increased during 
the 1973-93 period. Much of this research was basic in nature (influences of semiochemicals on host 
or prey selection; basic biology, physiology, and nutrition; development of mass production 
technology, etc.) There were, however, several pilot tests involving augmentation of specific 
biological control agents. Because of the large volume of material related to augmentation and 
conservation produced by ARS personnel during this period, an attempt to provide a comprehensive 
review will not be made here. Instead, discussions will focus on demonstrations of effectiveness and 
major new trends in basic research programs. It must be kept in mind that much of IPM research 
could be related to conservation of natural enemies. 


Parasites (parasitoids) and predators of crop pests. Lixophaga diatraeae, a tachinid parasite native to 
several Caribbean islands, has been used in augmentation programs against the sugarcane borer in the 
Caribbean region and South America (King et al. 1981). Yet, the effectiveness of this parasite had 
not been conclusively demonstrated (Bennett 1969). Thus in 1973, the ARS began evaluating the 
technical feasibility of using L. diatraeae to suppress sugarcane borer populations in Louisiana and 
Florida. King et al. (1979) developed a mass production technique for this parasite using greater wax 
moth larvae, which cost about 1/5 as much as using sugarcane borer larvae. Field parasitism of 
sugarcane borer larvae increased significantly after augmentative releases of L. diatraeae in 
Louisiana and Florida and suppression was apparent in some fields (Summers et al. 1976; King et al. 
1981). King et al. (1981) concluded that early-season releases of L. diatraeae may be useful against 
the sugarcane borer. Implementation of such a program, however, would require development of an 
inexpensive mass rearing technique, limiting parasite dispersal from release areas, establishing 
appropriate release rates, and an appropriate economic analysis. 


The eulophid Pediobius foveolatus was imported from India during the late 1960s by personnel of the 
Beneficial Insects Research Laboratory then at Moorestown, NJ (Angalet et al. 1968). This parasite 
of epilachnine beetle larvae was imported to attack the native American Mexican bean beetle. The 
parasite cannot overwinter in the U.S. The parasite attacks beetle larvae and has no diapause, while 
the Mexican bean beetle overwinters as an adult. In the early 1970s, an area-wide suppression 
program for the Mexican bean beetle in Maryland using inoculative releases and nurse crops of snap 
bean resulted in nearly 100% parasitization of beetle larvae and a four-fold reduction in insecticide 
usage (Stevens et al. 1975). An economic analysis by Reichelderfer (1979) of the USDA, 
Economics, Statistics, and Cooperatives Service, demonstrated that inoculative releases of P. 
foveolatus yield greater returns than do insecticide treatments. This augmentation program became 
one of the initial demonstration programs of the APHIS biological control programs discussed in 
Chapter VI, and is continuing in the northeastern United States, particularly in New Jersey. 


Edovum puttleri, another eulophid parasite, was imported from Colombia, South America in 1980 
and found to parasitize successfully eggs of the Colorado potato beetle (Puttler and Long 1983). Like 
P. foveolatus, this parasite does not overwinter in the U.S. and, thus, must be released periodically. 
Though Schroder and Athanas (1985) reported significant rates of parasitization on potato plants, E. 
puttleri has not been found to be effective on potatoes, apparently because of the way potato leaves 
lay on each other. However, E. puttleri is being used effectively in New Jersey to control the 
Colorado potato beetle on eggplant (Lashomb 1989). 


The genus Chrysoperla and other genera of the neuropteran family Chrysopidae includes a number of 
important insect predators, including Chrysoperla carnea and C. rufilabris. Both species are widely 
distributed in North America and C. carnea is found worldwide except for Australia. These two 
species are predaceous in the larval stage and attack a variety of pests including aphids, chinch bugs, 


61 


mealybugs, scales, whiteflies, leafhoppers, lepidopterous eggs and larvae, and mites (Hydorn 19745 
and references therein). Chrysoperla species have a number of attributes that make them ideal 
candidates for periodic release programs: 1) they feed on numerous pests and occur in many different 
agroecosystems; 2) when released as eggs or young larvae, these predators are unable to leave the 
target area; 3) they have high searching rates; and 4) larvae are tolerant to some insecticides. In the 
late 1960s and early 1970s, considerable work on C. carnea was conducted by personnel of the ARS 
Cotton Insects Research Laboratory in College Station, TX. Field releases of C. carnea significantly 
reduced Heliothis/Helicoverpa populations and damage (Ridgway et al. 1973, 1974; Ridgway and 
Kinzer 1974; Kinzer 1976), though high release rates were required. Rearing techniques at the time 
could not economically produce the numbers of Chrysoperla needed for control of these pests. Thus, 
from the mid 1970s until the late 1980s, research on Chrysoperla in ARS was limited. In 1990, 
Nordlund and Morrison reported on the predation behavior of C. rufilabris larvae. These studies 
demonstrated that this predator exhibits some success-motivated searching, particularly when feeding 
on tobacco budworm eggs, but that handling time did not decrease with experience. Also, tobacco 
budworm larvae were the preferred prey, when compared to cotton aphid or tobacco budworm eggs. 
Nordlund et al. (1991) demonstrated that C. rufilabris larvae would feed on Colorado potato beetle 
eggs and larvae and could provide control of populations in field cages. With the rising concern 
about the sweetpotato whitefly, Breene et al. (1992) showed that C. rufilabris can also control this 
major pest on greenhouse Hibiscus. 


Morrison and colleagues (Morrison et al. 1975; Morrison and Ridgway 1976; Morrison 1977; 
Elkarmi et al. 1987) worked on improving rearing techniques for these predators. The status of 
Chrysoperla mass rearing technology was reviewed by Nordlund and Morrison (1992). A number of 
commercial insectaries are currently producing C. carnea and C. rufilabris for use against a variety 
of pests using the basic technology developed at the Cotton Insects Research Laboratory. Efforts are 
currently underway at the Biological Control of Pests Research Unit in Weslaco, TX, to automate 
this rearing process (Nordlund and Morrison 1992). 


In 1981, the ARS initiated a pilot test "to evaluate on a large scale, in replicated field experiments, 
current technology for augmenting and manipulating Trichogramma populations to manage Heliothis 
[s. lat.] spp. in cotton." This project involved personnel from the Cotton Insects Research Laboratory, 
and the Pest Control Equipment and Methods Research Unit, College Station, TX; Southern Grain 
Insects Research Laboratory (now the Insect Biology and Population Management Research 
Laboratory), Tifton, GA; Southern Field Crop Insect Management Laboratory (SFCIML), Stoneville, 
MS; the Boll Weevil Eradication Research Unit, Raleigh, NC; Beneficial Insect Introduction 
Laboratory, Beltsville, MD; the University of Arkansas; and North Carolina State University. This 
pilot test provided an opportunity to test a number of the components including mass production and 
aerial release of a Trichogramma augmentation program. The studies conducted during this pilot test 
did demonstrate the ability to mass-produce Trichogramma, transport them to the field, release them, 
and increase rates of parasitization significantly. Unfortunately, boll weevil outbreaks in the study 
area resulted in the extensive use of insecticides, which had a negative impact on both the released 
Trichogramma and naturally-occurring predators and parasites. Thus, the results were not conclusive 
(King et al. 1985). This study did demonstrate, however, that high levels of parasitization can be 
produced with augmentative releases of Trichogramma. 


A number of other parasites for control of Heliothis/Helicoverpa spp. have been studied by ARS 
scientists. H. R. Gross, at the Insect Biology and Population Management Research Laboratory, 
Tifton, GA, did considerable work with the tachinid Archytas marmoratus for control of the corn 
earworm in corn (Gross 1988, 1990; Gross and Johnson 1985; Gross and Young 1984). This work 
demonstrated that significant increases in parasitization could be obtained with applications of 
mechanically extracted maggots or releases of adult insects. The braconid Microplitis croceipes also 
received considerable research attention. Workers from SFCIML, Stoneville, MS; Insect Biology and 


62 


Population Management Research Laboratory, Tifton, GA; Insect Attractants, Behavior, and Basic 
Biology Research Laboratory, Gainesville, FL; Biological Control of Insects Research Laboratory, 
Columbia, MO; and the Veterinary Toxicology and Entomology Research Laboratory, College 
Station, TX, cooperated in various aspects of this research (Powell et al. 1989). The inability to 
mass-produce these parasites economically is the major impediment to their utilization. (For 
Heliothis/Helicoverpa studies, see also King et al. 1989, and Tillman 1993.) 


Workers at the Biological Control of Insects Laboratory (later the Honey Bee and Insect Biological 
Control Research Unit) in Tucson, AZ, studied parasites for use in augmentation programs against 
lygus bugs. This work involved studies of the biology and ecology of Anaphes iole (=ovijentatus), an 
egg parasite, and Leiophron uniformis, which attacks nymphs (Debolt 1981, 1987, 1989; Jackson 
1982, 1986, 1987; Jackson and Graham, 1983; Graham and Jackson 1982; Graham et al. 1986; Jones 
and Jackson 1990; Norton et al. 1992). Here, too, the inability to mass-produce these parasites 
economically proved to be a major impediment to their use (Debolt 1987). 


In the late 1980s, workers at the Subtropical Agricultural Research Laboratory, Weslaco, TX, 
building on the previous work by J. R. Cate while he was at Texas A&M University, began working 
on augmentation programs against the boll weevil. The Lower Rio Grande Valley of Texas had an 
effective cotton stalk destruction program that generally held boll weevil populations to relatively 
low levels. Also, the Valley is a fairly small and isolated cotton growing region. The boll weevil, of 
course, is an exotic pest, originating in southern Mexico, where it is attacked by numerous parasites 
(Cross and Mitchell 1969; Cate 1985; Cate et al. 1990). Though research on classical biological 
control of the boll weevil has a long history, all attempts to establish exotic boll weevil parasites in 
the U.S. have been unsuccessful. Yet, Johnson et al. (1973) and Cate et al. (1990) reported 
significant increases in boll weevil mortality following releases of the pteromalid parasite Catolaccus 
grandis, indicating the possibility of using this exotic parasite in an augmentation program against 
the exotic boll weevil. Summy et al. (1991) and Morales-Ramos and King (1991) reported that such 
an approach is technically feasible, though work will be required to develop adequate mass 
production and efficient release techniques. 


Workers at the Tropical Fruit and Vegetable Research Laboratory in Honolulu, HI, have recently 
begun research on the possibility of augmenting parasites of fruit flies in Hawaii (Wong et al. 1991). 
They have been releasing over a million wasps per week of three braconid species, 
Diachasmimorpha longicaudata, D. tryoni, and Psyttalia fletcheri, against three tephritid pests, 
oriental fruit fly, Mediterranan fruit fly, and melon fly (Wong and Ramadan 1992). Also, work on the 
braconid parasite Biosteres arisanus, an egg-larval parasite, which can develop in at least seven 
species of tephritid pests, and on other parasites, is continuing (Ramadan et al. 1991, 1992). 


Parasites and predators in stored products. The stored product environment, in which losses due to 


insects amount to about 4 million tons of grain per year in the United States (Nilakhe and Parker 
1989), provides an ideal situation for augmentation. A number of parasites and predators that may be 
useful in stored products have been studied by personnel of the Stored Products Insects Research and 
Development Laboratory in Savannah, GA, and the Stored Products Insects Research Unit, Madison, 
WI. These include: Trichogramma pretiosum, Habrocytus cerealella, Anisopteromalus calandrae, 
Xylocoris flavipes, Bracon hebetor, and Pyemotes tritici (Arbogast 1979, 1984; Brower and Cogburn 
1989; Brower 1984 a and b; Brower and Press 1988, 1992; Burkholder 1981; Hagstrum and Smittle 
1977, 1978; Keever et al. 1986; LeCato et al. 1977; Press et al. 1975, 1977). Experiments in the 
laboratory and small scale warehouse studies have shown that the pteromalid parasite A. calandrae 
can effectively suppress populations of "grain weevils" (Sitophilus spp.), the parasites B. hebetor and 
T. pretiosum can be effective against lepidopterous pests in grain, and that X. flavipes, a generalist 
predator, can likewise be effective. Studies show that over 90% control can be achieved in single 
parasite-host or predator-prey systems (Brower and Cogburn 1989; Brower and Press 1992). 


63 


Commercial production and use of these biological control agents had begun and apparently was 
proving effective. Then in 1988, Food and Drug Administration (FDA) regulations relating to the 
addition of insects, even parasitic and predaceous insects, to food came into play; U.S. Marshalls 
"arrested" a bin of combine-run rye in Texas that had been treated with biological control agents 
(Maedgen 1989). This effectively put an end to the commercialization of this technology, at least 
temporarily. The regulations that mandated FDA's position have since undergone review and newly 
proposed regulations (Environmental Protection Agency, 1991) will, if adopted, permit use of 
parasitic and predaceous arthropods for biological control in stored products. Thus, research in this 
important area is continuing. 


Parasites and predators of insects affecting man and animals. Biological control of insect pests of 
man and livestock is an important component of the ARS research program. Weidhaas and Morgan 
(1977) of the Insects Affecting Man and Animals Research Laboratory (now the Medical and 
Veterinary Entomology Research Laboratory), Gainesville, FL, reviewed biological control of 
muscoid flies and selected species of mosquitoes. The house fly costs U.S. farmers approximately 
$100 million annually (Anonymous 1980), annual losses caused by the horn fly are $730 million, and 
for the face fly losses are in excess of $53 million (Drummond et al. 1981). 


Blume (1985) listed 43 species of parasitic Hymenoptera and Fincher (1990) listed 81 species of 
predators associated with insect pests in cattle dung in the U.S. Yet these important pests are seldom 
effectively controlled. One important factor contributing to this lack of control is that the parasitic 
and predaceous insects do not appear early in the season when fly populations begin to build up. This 
provides an opportunity for augmentation programs, and research is continuing (Summerlin et al. 
1984, 1990, 1991 a, b and c). 


The pteromalid Spalangia endius has advantages in augmentation programs over a number of other 
parasites that attack muscoid flies. For one thing, females search all levels of the manure, the major 
fly breeding site. The development time for S. endius is approximately twice that for house flies. 
While this long development time is probably one reason S. endius does not provide satisfactory 
control of house flies in nature, it makes the mass production, packaging, storage, and transportation 
activities associated with a periodic release program much easier. For example, Weidhaas and 
Morgan (1977) reported that parasitized fly pupae of different ages could be packaged together to 
give sustained release of parasites over a period of up to a week. Morgan et al. (1975a) conducted a 
preliminary experiment involving releases of S. endius in an enclosed building and eliminated a 
population of house fly. Morgan et al. (1975b) tested S. endius in a commercial poultry installation 
and 100% parasitism was observed after four weeks, and house flies were completely suppressed 
within 35 days. Morgan et al. (1976) released S. endius three times per week for five weeks (a total 
of 90,000 parasites) at a commercial dairy and reduced fly populations by 93%. This parasite is now 
available from a number of commercial sources. 


Work on S. endius and Muscidifurax zaraptor, a pteromalid wasp that attacks house fly pupae, was 
also conducted at the Midwest Livestock Insects Research Unit in Lincoln, NE, with particular 
emphasis on infield propagation (Pawson and Petersen 1989; Petersen 1989; Petersen et al. 1991, 
1992 a and b; Petersen and Watson 1992). 


There was also some additional work on dung beetle competitors of livestock pests during this period 
at the Veterinary Toxicology and Entomology Research Laboratory, College Station, TX (Fincher 


and Hunter 1986, 1989; Fincher et al. 1986; Hunter et a 1991). However, ARS efforts in this area 
have declined. 


Recent research by ARS and other U:S. scientists on the use of parasites, predators, and competitors 
for the control of livestock pests has been discussed in several comprehensive reviews (Science and 


64 


Education Administration 1981; Patterson and Rutz 1986; Drummond et al. 1988; Rutz and Patterson 
1990). 


Advances in rearing parasites and predators. Augmentation of entomophagous arthropods in the form 
of inoculative and particularly inundative releases is dependent on an ability to produce large 
numbers of high quality biological control agents at a relatively low cost (King and Morrison 1984). 
Rearing on natural or factitious hosts or prey can be very expensive. Thus, considerable interest in 
the development of artificial diets for predators and in vitro rearing techniques for parasites exists. 
Efforts by ARS in this area began at the Biological Control of Insects Research Laboratory at 
Columbia, MO, with in vitro rearing of Pteromalus puparum (Hoffman and Ignoffo 1974; Hoffman 
et al. 1973, 1975). Efforts to develop in vitro rearing techniques for Cotesia (=Apanteles) 
marginiventris and Microplitis croceipes were undertaken at the Insects Attractants, Behavior and 
Basic Biology Research Laboratory in Gainesville, FL (Greany 1980, 1981, 1986). At the Cotton 
Insects Research Unit in College Station, TX, work was begun by W. C. Nettles, Jr. on development 
of in vitro rearing techniques for the tachinids Eucelatoria bryani and Palexorista laxa, and for 
Trichogramma spp. (Nettles 1990) and is continuing at the Biological Control of Pests Research Unit 
in Weslaco, TX. Nettles has achieved 50% yield of adults with Eucelatoria. To date, at least 33 
species of parasites have been reared with varying degrees of success on artificial diets (Nettles 
1990). 


In regard to predators, artificial diets for Chrysoperla spp. were developed by Vanderzant at the 
Cotton Insects Research Laboratory at College Station, TX (Vanderzant 1969, 1973; Martin et al. 
1978). Research on development of artificial diets for Geocoris punctipes, a predaceous heteropteran, 
and other predators has been conducted at the Honey Bee and Insect Biological Control Research 
Laboratory at Tucson, AZ. This work is reviewed by Cohen (1992) and Cohen and Staten (1993). 
Guerra (1992) of the Subtropical Agricultural Research Laboratory, Weslaco, TX, reported on the 
development of diets for Bracon mellitor and Catolaccus grandis, parasites of the boll weevil, which 
are based on hemolymph of non-host insects. Adult yields were low, however; high larval mortality 
was attributed to non-dietary factors in the rearing process. Work to improve the diets and rearing 
system is continuing. (Anderson and Leppla 1992.) 


Semiochemicals to manipulate parasites and predators. One of the major new research efforts and 
one which developed considerable momentum during the 1973-93 period was on the use of 
semiochemicals to manipulate the host and prey selection behavior of entomophagous insects 
(Nordlund et al. 1981). Many entomophagous insects are dependent on semiochemicals to locate 
suitable habitats in which to search or to locate hosts or prey within the habitat (Vinson 1981; 
Weseloh 1981; Greany and Hagen 1981). Use of semiochemicals to increase the effectiveness of 
naturally occurring or released parasites or predators is environmental manipulation. 


Researchers had known for some time that Trichogramma evanescens females responded to chemical 
stimuli associated with the oviposition site of their hosts. Scientists at the Southern Grain Insects 
Research Laboratory (now the Insect Biology and Population Management Research Laboratory) in 
Tifton, GA, reported that 7. evanescens females responded to kairomones in the scales of corn 
earworm moths (Lewis et al. 1972). As the research program developed, a number of Trichogramma 
species, including 7. achaeae and T. pretiosum, were studied. This work initially demonstrated that 
the kairomone(s) in the moth scales could elicit increased rates of parasitization when applied to 
plots in the field (Lewis et al. 1975a). Lewis et al. (1975b) also demonstrated that this increase in 
parasitization was due to the inducement and continuous reinforcement of an intensive search 
behavior rather than attraction. This work continued and other parasites and predators, including 
Chrysoperla carnea, Microplitis croceipes, Cotesia marginiventris, and Telenomus remus, and the 
roles plant-produced compounds play in host selection have been studied (Dmoch et al. 1985; Lewis 


65 


et al. 1977, 1988, 1990; Nordlund and Lewis 1985; Nordlund et al. 1977, 1983, 1985, 1987, 1989; 
Tumlinson et al. 1993). 


ARS scientists at other locations also began working on semiochemicals influencing the behavior of 
entomophagous insects. Greany et al. (1977), of the Insect Attractants and Basic Biology Research 
Laboratory, at Gainesville, FL, found that Diachasmimorpha longicaudata, a parasite of fruit fly 
larvae, is attracted to acetaldehyde, a chemical produced by a fungus in rotting fruit. Personnel at the 
Cotton Insects Physiology Laboratory in Baton Rouge, LA, reported that Eucelatoria spp. are 
stimulated to larviposit by a kairomone found in tobacco budworm cuticles (Nettles and Burks 1977; 
Burks and Nettles 1978). The importance of semiochemicals in the host and prey selection behavior 
of parasites and predators was demonstrated and considerable insight into how they function was 
gained. However, to date, there has been no practical utilization of semiochemicals in applied 
biological control programs. 


Gross et al. (1975) found that prerelease stimulation of Trichogramma spp. and Microplitis croceipes 
resulted in significant increased retention of parasites in the release area and increases in 
parasitization. Use of prerelease stimulation could improve the effectiveness of release programs and 
is likely to be the first applied use of semiochemicals in biological control programs. 


Significant achievements in ARS's biological control augmentation/ conservation programs during 
1973-93. During this period, the technical feasibility of augmenting several parasites and predators 
was demonstrated. While this was being accomplished, some improved techniques for rearing, 
storing, transporting, and releasing several organisms were developed. Knowledge of the basic 
biology and ecology of numerous parasites and predators and of the mechanisms of host and prey 
selection was increased. 


It became abundantly clear that before augmentation in the form of inundative releases could be 
widely adopted, some major advances in the development of economical mass rearing systems were 
needed. Toward that end, ARS has increased the amount of research effort on the development of 
mass rearing techniques for entomophagous insects. 


2. Arthropod-Parasitic Nematodes. By W. R. Nickle, J. R. Coulson, P. V. Vail, J. E. Lindegren, and 
W. J. Schroeder. 


By 1972, personnel in the Nematology Investigations of ARS had increased to 28 SYs nationwide. 
Of these 27 conducted research on plant nematodes, and only one worked on insect nematodes; there 
were, however, several ARS entomologists also working with insect nematodes. After the 1972 
reorganization, the single insect nematologist, W. R. Nickle, became part of the new Nematology 
Laboratory of the Plant Protection Institute at the Beltsville Agricultural Research Center in 
Maryland. In November 1985, the nematode taxonomists of this Laboratory were administratively 
merged with other taxonomists to form the newly organized Systematic Botany, Mycology, and 
Nematology Laboratory (SBMNL) within an expanded Biosystematics and Beneficial Insects 
Institute (BBII) at Beltsville. In 1988, the BBII was disbanded, and in January 1989, the SBMNL 
became the Systematic Botany and Mycology Laboratory with the return of the nematode 
taxonomists to the Nematology Laboratory, both laboratories being part of the new Plant Sciences 
Institute at Beltsville organized in 1988. (See also section D below.) 


Nickle's work on the classification of mermithid nematodes (Nickle 1972), in which he described the 
infective stage of the mosquito nematode now known as Romanomermis culicivorax, enabled ARS 
entomologists studying control of mosquitoes at Lake Charles, LA, to develop techniques for 
mass-rearing the nematode. Research by ARS insect pathologists and entomologists, and Nickle's 
pilot test project in 1974, resulted in the commercialization of this nematode as a mosquito control 


66 


product, and the nematode is still used for mosquito control in some third world countries. In 1976 
and again in 1981, the Environmental Protection Agency determined that nematodes were classified 
as macroorganisms, exempting them from regulation as pesticides under the Federal Insecticide, 
Fungicide, and Rodenticide Act (FIFRA). (Ignoffo et al. 1973, 1974; Petersen 1975, 1980, 1984; 
Nickle 1976; Petersen and Chapman 1979; Nickle and Welch 1984.) 


A Hexamermis-type mermithid, known to kill up to 30% of gypsy moth caterpillars in the USSR, was 
imported from Europe and Japan in 1974-76 from the European and Asian Parasite Laboratories’ 
gypsy moth exploration programs, and the US-USSR biological control exchange program, and some 
were released in New Jersey (by Nickle and the New Jersey Department of Agriculture) and 
Pennsylvania (by the Pennsylvania Bureau of Forestry). This mermithid was apparently the first 
exotic insect-parasitic nematode purposely introduced into the U.S. (Drea et al. 1977; Coulson 
1981c; Schaefer and Ikebe 1982; Coulson and Soper 1989). 


High rates of parasitization by Hexamermis-type nematodes of the Colorado potato beetle were found 
in studies in the early 1980s by foreign scientists in Austria, and in explorations for parasites of corn 
rootworms by ARS scientists in Peru. These nematodes were studied by Nickle and were shown to 
have too wide a coleopteran host range, which included beneficial lady beetles, for introduction into 
the U.S., and the foreign material was destroyed. (Nickle and Kaiser 1984; Nickle et al. 1984; Kaiser 
and Nickle 1985.) 


Recent work by Nickle includes the description of a nematode parasitizing fire ants in Brazil (Nickle 
and Jouvenaz 1987) and joint studies at Beltsville with Steinernema-type nematodes for control of 
"mushroom flies" (Nickle and Cantelo, 1991). The fire ant nematode was discovered by scientists of 
the ARS Insects Affecting Man and Animals Research Laboratory at Gainesville, FL (now the 
Medical and Veterinary Entomology Research Laboratory), during explorations in Brazil, where it 
destroyed 25% of fire ant colonies there; plans include possible introduction of this nematode into 
fire ant-infested areas of the U.S. There are 88 CRIS projects that include work on Steinernema 
nematodes, of which about ten strains are known, and several other ARS nematologists are studying 
their use against various insect pests. 


Studies of insect-parasitic nematodes by other ARS scientists (entomologists) also included the 
discovery of a new species of nematode found attacking the tobacco flea beetle in North Carolina 
(Elsey and Pitts 1976; Elsey 1977), studies of nematodes attacking Spodoptera armyworms and 
wireworms in Washington (Howell 1979; Toba et al. 1983) and cucumber beetles in South Carolina 
(Creighton and Fassuliotis 1980, 1982; Elsey 1989, 1991; Schalk and Creighton, 1989), and work in 
Georgia with a nematode discovered in French Guiana parasitizing Spodoptera adults (Remillet and 
Silvain 1988). 


Some recent events important to the development of the use of insect-parasitic nematodes for 
biological control of insects include: 1) publication of several important reference works on the 
subject by University of California and ARS nematologists (Poinar 1979; Nickle 1984); 2) the 
Symposium on Entomogenous Nematodes held in 1980 at the annual meeting of the Society of 
Nematologists in New Orleans, the proceedings of which (Society of Nematologists, 1981) include 
papers by ARS scientists W. R. Nickle and J. J. Petersen; 3) the ARS Nematology Workshop held in 
1984 at Beltsville to discuss the status and future direction of ARS nematology research (USDA 
1984b); and 4) the joint development by ARS nematologists and entomologists of suggested 
guidelines for the importation and release of foreign insect-parasitic nematodes into the U.S. (Nickle 
et al. 1988). 


By 1989, ARS had an increased emphasis on biological control due to contamination of ground water 
by chemical pesticides. ARS now (1993) has about five SYs working on insect-parasitic nematodes, 


67 


mainly on steinernematids. J. E. Lindegren is working with nematodes for control of fruit flies and 
the pink bollworm, a cooperative California-Arizona project (Lindegren et al. 1990, 1992). M. G! 
Klein has studied nematodes on Japanese beetle grubs in Ohio. W. J. Schroeder has been in the 
process of developing nematodes for control of Diaprepes abbreviatus and other weevils (Pachnaeus 
spp.) affecting citrus roots in Florida since 1980; following a pilot test during 1989-91 (Schroeder 
1992), the commercial nematode product BioVector™ was released by Biosys, and the product was 
added to the citrus spray guide in Florida. G. Fassuliotis and C. S. Creighton continued work on 
nematodes of Diabrotica beetles in South Carolina, and C. E. Rogers and others continued studies on 
the new aphelenchid on Spodoptera in Georgia (Rogers et al. 1990). J. J. Jackson continued research 
on Steinernema and Heterorhabditis nematodes, including laboratory study of a species introduced 
from Argentina, on the western corn rootworm in South Dakota (Jackson and Brooks 1989). Nickle 
and W. W. Cantelo continued study of these nematodes on "mushroom flies" and Colorado potato 
beetles in Maryland (Nickle and Cantelo 1991; Cantelo and Nickle 1992). Nickle also worked on 
nematode delivery systems, taxonomy, and nematodes of corn rootworms (Nickle and Shapiro 1992; 
Connick et al. 1993). 


Additional recent research dealing with insect-parasitic nematodes by ARS scientists was identified 
in preparation of the following section on arthropod pathogens, and is summarized briefly here and in 
Appendix II. 


Much of the developmental work, such as on life cycles, taxonomy and rearing, had been completed 
by 1974 when research on this novel approach to insect control was undertaken by Lindegren. 
Further advancement toward commercial use did, however, require development of new or improved 
methods for nematode production, storage, application, selection for virulence, and quality control 
monitoring systems (Lindegren et al. 1979, 1993b; Hara et al. 1981). Some of the accomplishments 
include the development of application and monitoring techniques for the first commercial 
application of nematodes for control of carpenterworm in commercial fig orchards in California 
(Lindegren et al. 1981a; Lindegren and Barnett 1982); help in the establishment of the first 
commercial nematode production company in the United States, and similar consultation with 
subsequent companies; successful field applications of nematodes for control of the Colorado potato 
beetle, sugarbeet wireworm, "medfly", oriental fruit fly, and melon fly, with ongoing research on the 
Caribbean fruit fly, Fuller rose beetle, and pink bollworm (Toba et al. 1983; Lindegren and Vail 
1986; Lindegren et al. 1990, 1992); the development of a genetically selected, more virulent 
nematode called "Kapow" (Agudelo-Silva et al. 1987); and the development of a simple, dependable 
in vivo production method for laboratory and small scale testing (Lindegren et al. 1993b). 


Cooperative tests with the University of California Cooperative Extension Service and industry 
provided data on control of navel orangeworm with an entomogenous nematode (Agudelo-Silva et al. 
1987; Lindegren et al. 1978, 1981b, 1987). A nematode larvicidal soil drench was developed for 
reduction of Hawaiian fruit flies (Lindegren and Vail 1986; Lindegren 1990; Lindegren et al. 1990). 
Soil applications of the nematode Steinernema feltiae in field cages reduced larval populations of 
Colorado potato beetle and sugar beet wireworm by 71 and 29%, respectively (Toba et al. 1983). 
Searches in Brazil provided a nematode capable of invading fire ant queens that is highly destructive 
to its host and has the potential for eliminating established colonies (Nickle and Jouvenaz 1987). A 
sand barrier bioassay provided a measurement of host searching ability of various insect-parasitic 
nematodes, and showed a significant difference in host searching ability for three of the six 
nematodes tested; when evaluated at lower nematode concentrations, a new species of Steinernema 
from Texas and Mexico was the most effective host searching nematode (Lindegren et al. 1992, 
1993a). This new species (S. riobravis) shows great promise for controlling the corn earworm 
(Cabanillas and Raulston 1994 a and b; Cabanillas et al. 1994). And finally, as noted above, based on 
the findings of a joint ARS-University-Industry effort, the U.S. Environmental Protection Agency 


68 


exempted entomopathogenic nematodes from setting of a tolerance (exempt from registration) which 
promoted the testing, commercial production and sale of these organisms for insect control. 


3. Arthropod Pathogens. By P. V. Vail, R. A. Humber and J. R. Coulson 


After the reorganization of 1972, insect pathology research became the responsibility of the National 
Program Leader (NPL) in charge of Biological Control. However, most of the insect 
pathology/microbial control research was still conducted in commodity or problem area oriented 
laboratories. Exceptions included the Insect Pathology Laboratory at Beltsville, MD, and the 
Biological Control of Insects Research Laboratory at Columbia, MO. Thus, many of the pathology 
programs were within research units headed by other NPS members (i.e., cotton, grains, etc.) and the 
NPL for biological control had little input into these programs. Prior to the reorganization, ARS 
insect pathologists/microbial control scientists had annual research workshops which provided for 
information exchange between scientists as well as a mechanism for development of cooperative 
research projects. The last of these workshops was held in 1984 and thus a major coordination 
activity was lost. The opportunity for interaction between all insect pathologists and microbial 
control specialists to meet with interested NPLs as related to program goals was also lost. This forum 
has now been "taken over" by the Southern Regional Project 240 on developing insect pathology and 
microbial control agents. In the 1980s, the Insect Pathology Laboratory was placed into the new Plant 
Protection Institute at Beltsville, and was later renamed Insect Biocontrol Laboratory, with the 
addition of biological control entomologists from other laboratories at Beltsville (see section IVA). 
As with other disciplines, the number of insect pathologists has decreased due to program and budget 
constraints. However, it is believed that with the current concerns about misuse of chemical 
insecticides, emphasis on the development of microbial control agents should significantly increase 
both for production and postharvest pests. 


During the years 1973-93, significant advances were made in insect pathology/microbial control in 
both basic and applied areas. These are discussed in detail in Appendix II, with notes on 
administrative developments at the various involved locations. Only a summary of the more 
significant research advances is given here. 


Diseases and anomalies of the honey bee under continuous production and with different diets and 
amounts of pollen were investigated (Gilliam and Tabor 1973; Prest et al. 1974). This included one 
of the first reports of chalkbrood caused by Ascosphaera apis in honey bees in the U.S. Only larvae 
and prepupae would support the pathogen (Gilliam et al. 1978). Large variability in susceptibility 
was found between individual colonies and stressors were defined (Gilliam 1986). The alfalfa looper 
NPV host range continued to expand and its use in in vitro systems increased significantly. Genetic 
engineering of this virus for both agricultural and medical uses has made it one of the most 
thoroughly studied of all viruses. As one result of continuing studies at the Fresno, CA, location, a 
pathogen of nitidulid beetles was found to infect 15 species from six families and three insect orders 
and three species of mites (Kellen and Lindegren 1973, 1974). Osmotic studies of insect hemolymph 
(Adams and Wilcox 1973) aided in the development of new insect tissue fixatives and improvement 
of insect cell culture media. A granulosis virus was shown to control the imported cabbageworm 
(Hostetter et al. 1973). Pathogen autodissemination experiments were conducted with Trogoderma 
glabram using pheromone contamination sources, a method later recommended for population 
reduction (Burkholder and Boush 1974). Similar studies were conducted with Indianmeal moth and a 
granulosis virus (Kellen and Hoffmann 1987; Vail et al. 1993). 


Cooperative studies between Brazil and the United States led to the discovery of a fire ant pathogen 
which further stimulated interest in biological control for this important organism (Knell et al. 1977). 
The first reports of spiroplasmas led to their isolation from a number of insects including bees, 
wasps, beetles, flies and butterflies (Clark 1982). A non-occluded virus of Culicoides cavaticus 


69 


caused mortality rates of 70-90% in field collected larvae (Clark and O'Grady 1975). Based on 
research at Manhattan, KS, Bacillus thuringiensis was registered as a protectant for stored grains 
(McGaughey 1975b, 1976, 1978, 1980, 1982). Similar results were obtained with a granulosis virus 
(Kinsinger and McGaughey 1976; McGaughey 1975a, 1983). During these studies McGaughey 
discovered the potential for resistance to Bacillus thuringiensis in stored product pests (McGaughey 
1985, McGaughey and Beeman 1988). 


Research on formulations and adjuvants continued to extend the field activity of Bacillus 
thuringiensis and viruses (Hostetter et al. 1975, 1982; Bell and Kanavel 1978; Bell and Romine 
1980; Dunkle and Shasha 1988; Bartlett et al. 1990; McGuire et al. 1990; McGuire and Shasha 
1990). A large research program on the use of Nomuraea rileyi showed that this pathogen could be 
used as a prophylactic agent when directed towards early instars (Ignoffo 1981; Ignoffo and Garcia 
1985). Significant reduction of grasshoppers resulted from the treatment of 37,312 ha of rangeland 
with Nosema locustae (Henry and Onsager 1982). In early experiments to determine the feasibility of . 
area wide suppression methods, it was found that control of cabbage looper on cotton with a 
baculovirus could influence future population levels on lettuce (Vail et al. 1976). Bell and Kanavel 
(1976) conducted important investigations on methods of transmission of cytoplasmic polyhedrosis 
virus of the pink bollworm which led to large increases in production at the APHIS Pink Bollworm 
Mass Rearing Facility in Phoenix, AZ. An entomopathogenic fungal collection started by R. S. Soper 
and continued by R. A. Humber led to the world's foremost collection of these organisms 

("ARSEF"), which is located at Ithaca, NY. As of 1991, over 3,200 isolates of over 250 species are in 
the collection (Humber 1992). The importance of timing and adequate volume in the use of Bacillus 
thuringiensis for navel orangeworm control was demonstrated by Kellen et al. (1977). The first virus 
from fire ant was discovered in collections from Brazil by Avery et al. (1977). Additional pathogens 
from this insect were described by Banks et al. (1985) and Jouvenaz et al. (1980). Two forms of 
virions were recognized in baculoviruses which had important implications in understanding the 
pathology, cell culture and use of these organisms (Adams et al. 1977; Adams and McClintock 

1991). 


Research on comparative susceptibility of tobacco budworm/corn earworm showed the latter to be 
about ten times less susceptible to the alfalfa looper MNPV regardless of the inoculation method 
(Vail et al. 1978, 1982; Vail and Collier 1982). These studies pointed to the importance of knowing 
which of these species or proportions thereof were infesting fields. A large field test in El Salvador 
with microbial agents resulted in the near eradication of an anopheline mosquito malarial vector 
(Petersen et al. 1978a, 1978b; Willis et al. 1980). More simplified and efficient rearing procedures 
for gypsy moth led to a large scale production plant which produced over 1.5 million insects in a 
100-day period, yielding 50,000 ac equivalents of the gypsy moth NPV. Costs were reduced at least 
10-fold in the process (Shapiro and Bell 1981; Podgwaite et al. 1983). In 1980, Nosema locustae 
became the first protozoan registered as a microbial insecticide in the U.S. by the Environmental 
Protection Agency (Henry 1981). Bacillus thuringiensis was the first microbial registered for use on 
stored grain as a result of many of the studies conducted at the ARS Manhattan, KS, laboratory 
(McGaughey 1986). ARS, together with the Australian Commonwealth Scientific and Industrial 
Research Organization (CSIRO), played a key role in successfully introducing a pathogenic fungus 
of the spotted alfalfa aphid in Australia (Milner and Soper 1980; Milner et al. 1982). The first serum 
free insect cell culture medium (gypsy moth) that supported serial replication cycles of a baculovirus 
was developed (Goodwin and Adams 1980). Ascosphaera aggregata was shown to be the causative 
agent of chalkbrood of the alfalfa leafcutting bee and the epizootiology of the disease was established 
(Vandenberg and Stephen 1982; Stephen et al. 1981). In cooperation with the University of 
California, Berkeley, the first known occurrence of a calicivirus in an insect was reported (Kellen 
and Hoffmann 1982; Hillman et al. 1982). Two forms of the virus were described (Hoffmann and 
Hillman 1984). Later studies (Kellen and Hoffmann 1982) described the symptoms of the virus and 
described it as the "chronic stunt virus." Various adjuvants were discovered to increase the field 


70 


persistence or activity of baculoviruses such as sun screens, microencapsulation and boric acid 
(Tompkins et al. 1988; Shapiro and Bell, 1982). 


During the 1970s and 1980s, insect cell culture became a useful tool in the study of insect pathogens 
(baculoviruses). Scientists at ARS laboratories, primarily at Beltsville, MD, Gainesville, FL, 
Columbia, MO, and Fargo, ND, developed cell lines for this purpose from several major agricultural 
pests. Among the many lepidopterous pests from which cell lines were developed are fall armyworm 
(Vaughn et al. 1977; Lynn and Oberlander 1983), bollworm (Goodwin et al. 1982; McIntosh and 
Ignoffo.1983; McIntosh et al. 1983), tobacco budworm (McIntosh et al. 1981), cabbage looper 
(Goodwin et al. 1973; Lynn et al. 1982; Rochford et al. 1984), and tobacco hornworm (Eide et al. 
1975). Cell lines have also been developed from southern corn rootworm (Lynn and Stoppleworth 
1984), boll weevil (Stiles et al. 1992), Indianmeal moth (Lynn and Oberlander 1983), diamondback 
moth (Quhou et al. 1983), and navel orangeworm (Hoffman et al. 1990). 


The feasibility of applying entomopathogens in irrigation water was demonstrated (Hamm and Hare 
1982). Genetically controlled hygienic behavior of worker bees was shown to aid in control of 
chalkbrood in the honey bee (Gilliam et al. 1983). Quality control procedures were developed to 
preclude contamination of alfalfa looper NPV preparations by a calici-like virus (Morris et al. 1981; 
Vail et al. 1983). Formulation, treatment parameters and a method for disbursing Bacillus 
thuringiensis israelensis were developed for control of black flies. A UV tolerant gypsy moth NPV 
biotype was selected (Shapiro and Bell 1984). The first report of Bacillus thuringiensis crystal 
proteins toxic to muscid flies was reported by Temeyer (1984). Studies continued on the use of 
fungicides to control chalkbrood of alfalfa leafcutting bees; captan was shown to be effective as a 
dust in nest shelters (Parker 1984, 1985, 1987, 1988; Mayer et al. 1990). Researchers in Florida 
discovered that a copepod was an intermediate host for a protozoan pathogen of mosquitoes 
(Sweeney et al. 1985). This finding finally completed the known life cycle of one of the most 
common microsporidian in mosquitoes and other biting flies. A new group of viruses (ascoviruses) 
was found in fall armyworm, corn earworm and tobacco budworm, which was readily transmitted by 
a parasite but only moderately infective per os (Hamm et al. 1985, 1986). McCabe and Soper (1985) 
developed and patented a widely used process to dry mycelial mats for application of fungi as 
microbial control agents. A new production/formulation of the Indianmeal moth virus was developed 
(Cowan et al. 1986) and later patented (Vail 1991) which could reduce damage in raisins to the point 
of being of no economic consequence. Hamm et al. (1988) reported the first baculovirus infectious to 
a parasite which pointed out the need to diagnose imported or mass-produced beneficials when used 
for field release or research. During studies of introduced Entomophaga (as Entomophthora) grylli, it 
was discovered that sun-basking by grasshoppers may raise their body temperature above that 
required for development of pathogens (Carruthers et al. 1988b). Larkin et al. (1988) developed a 
program for the rapid construction of simulation models which was instrumental in guiding and 
evaluation of epizootiological studies on grasshopper pathogenic fungi (Carruthers et al. 1988a). 


A cooperative ARS-APHIS biological control of rangeland grasshoppers program utilizing an 
introduced Entomophaga fungus was conducted beginning in 1989 (Hostetter et al. 1993). This 
program and the successful establishment of the Australian fungus in North Dakota generated 
considerable controversy over the ecological significance of introducing exotic natural enemies 
against native pests in the U.S. (Lockwood 1993 a and b; Carruthers and Onsager 1993). 


In 1990, a large scale pilot test was initiated to determine the feasibility of using a nuclear 
polyhedrosis virus for control of early season populations of Heliothis/Helicoverpa over large areas 
of the Mississippi Delta (Bell 1990a, 1990b, 1991; Bell and Scott 1989; Bell et al. 1992). Granulosis 
virus infections were shown to influence hormonal titers in an insect host (Dougherty et al. 1989). A 
theoretical paper described the biophysical/biochemical basis for the process of germination in 
protozoa (Undeen 1990). An endophytic relationship was described between the corn plant and an 


at 


entomopathogenic fungus, Beauveria bassiana, in which the pathogen moves within the plant to 
control European corn borer (Bing 1990; Bing and Lewis 1991; Lewis and Bing 1991). A massive 
mortality of gypsy moths was inferred to have been caused by a fungus released 80 years earlier 
(Hajek et al. 1990). 


A more virulent biotype of the gypsy moth NPV was obtained after serial passage through its host; 
this new biotype was patented by ARS and the scientists involved (Shapiro et al. 1992). Research on 
fluorescent brighteners as protectants for baculoviruses led to the granting of a U.S. Patent 
05,124,149 (Shapiro et al. 1990). Both were licensed to private corporations for further development. 
Several pathogens including three fungi and a nematode were demonstrated to reduce sweetpotato 
weevil populations (Chalfant et al. 1990). Beauveria bassiana was shown to be effective against the 
boll weevil when used as a prophylactic treatment (Wright and Chandler 1990, 1991, 1992). Stephen 
and Fichter (1990a, 1990b) successfully selected for alfalfa leafcutting bee resistance, probably 
polygenic, to chalkbrood. McIntosh (1991) demonstrated that the celery looper NPV also had a wide 
host range in vitro and suggested that these systems could serve as rapid determinants of host range 
of natural viral isolates. Crystal protein genes of Bacillus thuringiensis israelensis, a pathogen of 
Diptera affecting man and animals, were cloned in Escherichia coli at Kerrville, TX, in 1991 (see 
Appendix II). Pink bollworm was demonstrated to be susceptible to several entomopathogenic 
nematodes (Lindegren et al. 1992). A rare protozoan, Malpighamoeba mellificae, was found to be 
causing severe population losses in the honey bee (Wilson and Collins 1992). 


As noted in Chapter I (section A.3), a Japanese fungal pathogen of gypsy moth was introduced into 
Massachusetts in 1910-11 (Speare and Colley 1912), without apparent successful establishment. This 
fungus, later described as Entomophaga maimaiga (Soper et al. 1988), was nearly forgotten until 

R. S. Soper (then at the Insect Pathology Research Unit, ARS, Ithaca, NY) collected it in Japan in 
1984 and began new studies of its potential to control gypsy moth (Shimazu and Soper 1986). It was 
released experimentally in the field in New York in 1985 and Virginia in 1986 (Reardon and Hajek 
1993). A fungus causing considerable mortality of gypsy moth larvae across the northeastern U.S. 
during 1989-90 proved to be E. maimaiga. Because the causative fungus was biochemically 
indistinguishable from Japanese strains of E. maimaiga, and because no modern introductions of E. 
maimaiga were made in the specifically affected regions, it was inferred that the massive mortality of 
gypsy moth must have been caused by the fungus introduced 80 years earlier by Speare and Colley 
(Hajek et al. 1990). Though that is not altogether certain (Hajek et al. 1995), the Japanese fungus is 
proving to be an effective control agent for the gypsy moth in the northeastern U.S. See Appendix II, 
section on Ithaca, NY. 


Another significant step in classical biological control occurred in 1981 with the establishment for 
the first time of an insect pathology component in the biological control exploration program at the 
ARS European Parasite Laboratory (EPL) in France. This began first by means of a cooperative 
agreement between the EPL and the French Institute Nationale de la Recherche Agronomique 
(INRA). The insect pathology program became an integral part of the ARS program by the time of 
the consolidation of the ARS European laboratories in Montpellier in 1991 with the assignment of 
L. A. Lacey. His principal duties are foreign exploration for entomopathogens of selected U.S. insect 
pests. Collections over a broad geographical area ranging from Spain to Nepal have been made. 
Many isolates have been obtained, but few have as yet been investigated for their potential as 
microbial control agents. See section B.1.a and Appendix II. The use of insect pathogens in classical 


biological control, though not new, increased in the U.S. in the latter part of this period (see Maddox 
et al. 1992). 


In addition, ARS insect pathologists were involved in several exchange agreements between the 
United States and the Soviet Union and People's Republic of China, some of which are noted in 


section B.1 of this chapter. These involved exchange of scientists, research information, and 


a2 


microbial cultures (Ignoffo 1979; Ignoffo et al. [1980]; Wong [1982]; Soper et al. 1992). And, an 
ARS insect pathologist also performed research in regard to microbial control of the Japanese beetle 
in the Azores, after the discovery of that pest in those islands (see Appendix II). 


C. BIOLOGICAL CONTROL OF WEEDS 


1. Invertebrate Natural Enemies of Weeds. By L. A. Andres, J. R. Coulson, T. D. Center, C. E. 
Turner, and C. J. DeLoach 


The period 1973-93 saw first the addition of new ARS laboratories and personnel devoted to 
classical biological control of weeds by introduction of insects and mites (Andres and Kok 1981), but 
toward the end of the period this trend was reversed. The expanded interest in the use of plant 
pathogens for weed control that also occurred during this period, is discussed in the following section 
(C.2). Though an active program for introduction and release of arthropod natural enemies continued, 
the work was severely hampered by several administrative changes plus questions of conflicting 
ecological interests. Most of these problems and questions also affected programs dealing with weed 
pathogens. 


A major problem concerned the coordination of research activities. The ARS classical biological 
control of weeds program was adversely affected by the 1972 ARS reorganization as was the ARS 
classical biological control of insects program. Discussions of the effects of this reorganization in 
regard to abolishment of the Insect Identification and Parasite Introduction Research Branch (IIPI) 
and thus the end of centralized leadership and coordination of ARS classical biological control 
research, the development of National Research Programs (NRPs) and National Program Leaders 
(NPLs), the formation of Working Groups, Technical Advisors, the International Activities office, 
and NPS matrix teams to attempt to coordinate ARS classical biological control programs for both 
insects and weeds, are included in sections A and B.1 in this chapter. 


Although the impact on the biological control of weeds program was not immediately apparent due to 
a number of newly released or promising agents in the introduction pipeline, the 1972 dissolution of 
the IIPI had a severe ongoing effect on the coordination of the study and importation of exotic natural 
enemies of weeds. This is perhaps even more severe than in the biological control of insects program. 
Weed projects often continue for ten or more years, which necessarily entails long-term coordination 
of the exploratory and research activities of the overseas laboratories with the domestic locations. 
This involves joint development of project plans and assignment of responsibilities; joint preparation 
of petitions and proposals for the importation and release of new candidate agents; the interchange of 
domestic and foreign stocks of the targeted weed to verify identification and acceptance by the 
foreign natural enemies; interchange of overseas and domestic researchers to facilitate pooling of 
information and skills; collecting and supplying to the overseas and North American cooperating 
laboratories native or rare and endangered test plants for host specificity tests; and coauthoring of 
reports and publications; etc. 


The IIPI formed a single administrative/technical unit for coordinating and directing the domestic 
and overseas research and importation program and apportioning and optimizing resources. 
Following the split of administrative and technical direction into two separate lines of responsibility, 
considerable effort was spent to devise ways of coordinating these two aspects to maintain national 
program coordination, as well as of addressing other problems noted below. The responsibility for 
day-to-day administration of ARS domestic biological control of weeds programs became scattered 
among those line managers in whose areas of responsibility the pertinent domestic laboratories were 
located. The administration of the foreign program, on the other hand, shifted to the international arm 
of ARS, i.e., the International Program Division until 1981, and since then the International 
Activities Office (now Office of International Research Programs). Since 1973, technical direction of 


73 


the overall national ARS biological control of weeds program was totally apart from the 
administrative elements, and rested with the ARS National Program Staff (NPS), and, until 1981, 
with Technical Advisors. This responsibility was shared by the incumbent NPLs for biological 
control, when one existed (see sections above), and the NPLs for weed research, which presented an 
opportunity for conflicting views concerning program needs, etc. As noted above, Technical 
Advisors (TAs) were appointed to assist the NPS in program coordination, from 1973-81; L. A. 
Andres, Research Leader of the Albany, CA, laboratory, was TA with primary advisory 
responsibility for the overseas program in Europe (the Rome laboratory), and C. J. DeLoach, 
Research Entomologist, Temple, TX, was TA with advisory responsibility for the program in South 
America (the Argentine laboratory); both also served as Technical Advisors for pertinent domestic 
aspects of the research program. In 1981, an NPS Biological Control Matrix Team was established 
and assumed responsibility for the technical planning and coordination of the ARS biological control 
program. 


As discussed in above sections, the ARS Working Group on Natural Enemies of Insects, Weeds and 
Other Pests (WGNE) was formed in 1973 in an effort to maintain national coordination of ARS 
biological control programs, including those devoted to weed control, but this group ceased to 
function after 1979. Other coordination efforts included the various workshops and meetings 
mentioned in previous sections. Although the Technical Advisors and the WGNE could prioritize 
research needs, the implementation of their recommendations, as well as those generated at these 
workshops and meetings were quite limited. The administration and coordination of classical 
biological control of weeds research processes and associated protocols remained cumbersome at 
best. 


Research on new biological control agents and their clearance for introduction into the United States 
continued to require close cooperation between domestic and overseas researchers. This included 
quarantine studies and handling of exotic natural enemies, release clearance by state and federal 
authorities, and finally, distribution, field release, and follow up evaluation studies. The success of 
the ARS biological control of weeds program led to the addition of new state and university 
biological control personnel to handle the cleared control agents. Unfortunately, the demand by these 
new state/university personnel and by the public for ever increasing numbers of organisms to release 
against their rangeland weeds led to federal-state coordination difficulties. ARS research efforts were 
in part diluted by efforts to collect, clear, and distribute agents to meet this rising demand (Andres 
and Kok 1981). APHIS' interest in biological weed control and establishment of laboratories at 
Mission, TX, and Bozeman, MT, (see Chapter VJ), for the importation and distribution of new and 
established weed control agents in the 1980s, provided relief in regard to the weeds of interest to 
APHIS; some funding for ARS overseas studies on those weeds was provided by APHIS. However, 
this added a second federal agency to the weed program, further compounding coordination 
problems. Retirements and relocations of research personnel, and changing NPS personnel of varying 
backgrounds and interests directing the technical aspects of the program, brought the former closely 
coordinated U.S. and Canadian biological control of weeds programs to a state of disarray (Harris 
1990). 


Another problem facing the weed program lay in the area of setting target weed priorities. Although 
several attempts were made to establish logical priorities in the weed program, much depends on 
funding sources and factors outside the scientists’ realm (e.g., political factors). Weed priorities in the 
Northeastern Region were established in the early 1970s by a regional biological control working 
group, and an attempt to establish national priorities was made at the 1984 ARS Research Planning 
Conference (USDA 1984a). Although these and earlier priorities were established without the benefit 
of much pertinent economic information, they did earmark principal weeds of regional and national 
importance. To assure that limited ARS resources were focused on projects of national interest as 
more ARS personnel became involved in biological control of weeds during the late 1970s and the 


74 


1980s, the assembling of data on economic losses due to specific weeds was encouraged to justify the 
selection of target weeds for new research projects. However, the difficulty in obtaining this 
information, which was extremely limited in regard to the weeds most amenable to biological control 
such as many pasture and rangeland weeds, and the general absence of strong user group support for 
many weeds, slowed the targeting of new projects. The lack of economic data also hampered ongoing 
projects when potential economic versus ecological questions arose in conjunction with the 
introduction of control agents. In the 1970s, a priority request for studies of the arthropod fauna 
associated with several narcotic plant species diluted overseas research efforts on biological control 
of rangeland weeds, and further interfered with the technical direction of the foreign program. On the 
other hand, the influx of narcotics program funds resulted in establishment of a new quarantine 
laboratory in Stoneville, MS (see below), which, however, by 1993, was non-functional for classical 
biological control of weeds, and strengthened the overall biological control of weeds program, at 
least temporarily (see Epilogue, section A). 


Other problems concerned potential conflicts of interest associated with targeted weeds and 


clearance of new biological agents for release in North America. The passage of the National 
Environmental Policy Act of 1969, and the Endangered Species Act of 1973, and subsequent 


regulations, severely impacted the biological control of weeds program. The often conflicting factors 
contributing to a slowdown of the program were: 1) differing views among the public and scientific 
community over the potential economic benefits and losses caused by specific weeds; and 2) 
increased concerns of environmentalists, ecologists, and weed researchers themselves that introduced 
weed control agents might impact native, non-target plants closely related to the target weed (Andres 
1981). These concerns translated into increased care in selecting plants for host specificity testing of 
proposed agents and, more importantly, increased the test time and logistical problems encountered 
in locating and culturing native plant species for the tests (Pemberton 1986; Turner 1986; Coulson 
and Soper 1989; Coulson et al. 1991). Eventually a testing strategy was developed that recognized 
these concerns and permitted a balanced assessment of the candidate agent's host range potential, 
allowing the introduction of the safest agent first. The testing of closely related native plant species 
became routine protocol (Pemberton 1986; Turner 1986). 


The interagency Working Group on Biological Control of Weeds established in 1957 (see Chapter 
III, section B) proved ineffective in resolving conflicts of interest regarding weeds targeted for 
research and in dealing with the questions raised regarding potential impacts on native plants of 
agents proposed for introduction. In an attempt to improve upon this situation, the interagency 
Working Group was disbanded and a Technical Advisory Group (TAG) on Biological Control of 
Weeds was created in 1987 to make recommendations directly to APHIS-PPQ, the agency 
responsible for issuance of U.S. importation and release permits; an official of the APHIS-PPQ 
permit office served as Executive Secretary of the TAG (Coulson and Soper 1989; Coulson 1992a). 
Unfortunately, due to implementation and coordination problems in the review process, TAG's 
responses to petitions were not always provided on a timely basis, and questions remained as to 
means of handling conflicts of interest, differences in Canadian and U.S. release standards, etc. 


The TAG, and the interagency Working Group before it, reviewed pre-release study data for 
adequacy and safety, and also reviewed background data on natural enemies proposed for release in 
Canada. Recommendations on Canadian proposals were advisory only. This led to confusion when 
concurrence was granted for release in Canada but denied in the U.S. until additional tests were 
carried out. Representatives of states bordering Canada and infested with the same weed species 
questioned those procedures, as did ARS researchers who felt some of the agents released in Canada 
might pose a threat to plants of ecological importance in the U.S. 


In 1993 efforts were begun in APHIS to reconstitute this advisory group, including the drafting of a 
new charter, to help make the group more effective in assisting in the evaluation of proposed 


75 


introductions of exotic weed control agents in the U.S.; this was part of a larger effort in APHIS to 
revamp all pertinent regulations and procedures for approving introductions of all exotic biological 
control agents. 


Since 1973, research at the ARS Biological Control of Weeds Laboratory in Italy focused on the 
following target weeds: field bindweed (1973-88); musk thistle and yellow starthistle (1973-present); 
Dalmatian toadflax (1974-79); leafy spurge (1974-present); diffuse knapweed (1975-present), curly 
dock (1977-83), and smooth bedstraw (1982-83), in addition to miscellaneous studies and collections 
of natural enemies of Eurasian watermilfoil, rush skeletonweed, Canada and Italian thistles, 
velvetleaf, Russian knapweed, spotted knapweed, and tansy ragwort. As noted above, during the 
years 1973-77, the laboratory was also directed to study the natural enemies of opium poppy (Rizza 
et al. 1980; Buckingham et al. 1983b). Research Leaders of the laboratory during this period have 
been G. R. Buckingham (1973-77), N. R. Spencer (1977-81), P. H. Dunn (1981-88), and L. Knutson 
(1988-91). The field bindweed and yellow starthistle projects were the focus of University of 
California scientists, but when these same scientists were hired as federal employees, the projects 
shifted to ARS. A substation was established in Greece in 1980 for study of the natural enemies of 
yellow starthistle, and studies of additional weeds were added later to the substation's program. And 
in 1981, the Rome laboratory was moved from its originally established location to expanded 
quarters outside of the city. 


As discussed in section B.1.a, several efforts were made during this period to consolidate the Rome 
and Paris laboratories at a single European location. This was finally accomplished in 1991, with the 
establishment of the European Biological Control Laboratory (EBCL) at Montpellier, France, under 
the direction of L. Knutson. Satellite locations were retained in Italy and Greece. Explorations by 
Rome and Montpellier personnel have ranged from locations in Europe and the former Soviet Union 
to China. Weed research at the EBCL and satellites continued to concentrate on leafy spurge, yellow 
starthistle and knapweeds in 1991-93, and studies of saltcedar were begun in cooperation with the 
ARS laboratory in Temple, TX (see below). Most of the natural enemy studies at the European 
laboratories were done in close cooperation with personnel at the Albany, CA, laboratory, and the 
agents were eventually shipped to that laboratory. However, since 1988, importations have also gone 
to the ARS locations at Temple, TX, and Bozeman, MT, for further study and release, and to APHIS 
personnel at Mission, TX, Albany, CA (1988-90 only), and Bozeman, MT, and to Montana State 
University scientists at Bozeman; see discussion of the ARS locations below. Several species were 
also sent to cooperators at Virginia Polytechnic Institute and State University, Blacksburg, VA, and 
the Maryland and New Jersey Departments of Agriculture (musk thistle insects). Natural enemies of 
curly dock and smooth bedstraw were studied briefly for the ARS laboratories at Stoneville, MS, and 
Beltsville, MD, respectively (see below). A high level review of the Rome laboratory program was 
held near Paris in October, 1983 (see also section B.1 above), which resulted in limiting the number 
of the laboratory's target weeds to one per scientist, all of which were to be deemed of national 
importance; see discussion above regarding establishing priorities for target weeds. The important 
reference/voucher collection of weed insects collected and studied during the Rome research 
program (1959-91) was recently organized, and records computerized. A plant pathology research 
program was initiated at the Rome laboratory in 1989, assisted by the temporary placement there of a 
scientist funded by the ARS laboratory at Frederick, MD (see section C.2 below). For references to 
some of the studies on weeds during this period at the Rome and Montpellier laboratories and 
substations, see: Dunn and Rizza 1977; Frick 1977; Boldt and Campobasso 1978; Kok et al. 1979; 
Pecora and Rizza 1980; Pemberton and Hoover 1980; Rosenthal 1981; Spencer 1981; Rosenthal and 
Buckingham 1982; Rizza and Pecora 1984; Sobhian and Zwélfer 1985; Maddox and Sobhian 1987; 
Clement et al. 1988; Dunn and Knutson 1989; Clement 1990, 1994; Fornasari and Knutson 1990; 
Castagnoli and Sobhian 1992; Pecora et al. 1992 a and b; Sobhian et al. 1992 a and b; Sobhian 1993 
a and b; Boldt and Sobhian 1993; Fornasari 1993; Fornasari and Pemberton 1993; Fornasari and 
Sobhian 1993; Fornasari et al. 1994. 


76 


During 1973-93, research at the ARS Biological Control of Weeds Laboratory in Argentina, under 
the leadership of C. J. DeLoach (1973-74) and H. A. Cordo (1974-present), focused on the following 
target aquatic weeds: waterhyacinth (1973-81), waterlettuce (1973-78), and waterprimroses and other 
aquatic weeds (1973-79); natural enemies resulting from these studies were designated for further 
study by the ARS laboratories in Florida (see below). As noted above, C. J. DeLoach was appointed 
Technical Advisor for this laboratory in 1974, and research in Argentina was subsequently begun on 
some of the target weeds of the new Temple, TX, laboratory, to which DeLoach was reassigned (see 
below); these included the native shrubs: mesquites, broomweeds and snakeweeds, creosotebush, 
Baccharis spp., "bitterweeds", Texas whitebrush, and other southwestern range weeds and brush 
pests, from 1976 to 1993. A few studies were also conducted during this period on natural enemies of 
pasture and row crop weeds (prickly sida, cockleburs, hemp sesbania, and smallflower galinsoga) for 
ARS laboratories in Mississippi and Maryland, as well as of a few insect pests (see section B.1.a 
above). In a striking example of cooperation that exists between ARS overseas scientists and local 
scientists, ARS and Argentine scientists cooperated in the introduction of insects already tested and 
established in the U.S. into Argentina for musk thistle and rush skeletonweed, and in the publication 
of a book on the potential of biological control of weeds in Argentina; the latter study analyzed the 
biological control potential of all the major Argentine weeds, discussed theory and methodology, 
work done in other countries, and the availability of natural enemies (DeLoach et al. 1989). For some 
other references to work at the Argentine station during this period, see DeLoach and Cordo 1976, 
1978, 1983; DeLoach et al. 1976, 1980; Cordo et al. 1978, 1981 1984; Cordo 1986; Cordo and 
DeLoach, 1975, 1982, 1987, 1992, 1993; see also references cited in the discussions below of the 
Temple, TX, laboratory, and significant accomplishments during this period. By the end of 1993, the 
mission of this laboratory, renamed the South American Biological Control Laboratory, was altered 
to target primarily insect pests (see section B.1.a above), with snakeweeds (Gutierrezia spp.) 
remaining the only target weed for the station (H. A. Cordo, pers. commun., 1993). 


In 1989, a third overseas biological control of weeds laboratory was established, in Queensland, 
Australia, by J. K. Balciunas (University of Florida collaborator, first employed by ARS in 1989), for 
the study of invertebrate natural enemies of aquatic and wetland weeds. This facility, called the 
Australian Biological Control Laboratory from 1989, originated as a University of Florida laboratory 
in 1985, and was initially made a satellite location of the ARS Fort Lauderdale, FL, laboratory (see 
below). In 1991, it was placed under the administration of the ARS International Activities office 
(now the Office of International Research Programs, OIRP) in Beltsville, MD, together with all other 
ARS overseas laboratories. Targets of research there have been the aquatic and wetland weeds 
hydrilla and melaleuca, but were restricted to the latter in 1992. (Balciunas and Purcell 1991; 
Balciunas and Burrows 1993; Balciunas and Chen 1993; Balciunas et al. 1993 a and b.) 


In an effort to develop a flow of effective weed natural enemies from the Ukraine, Caucasus, and 
central and eastern Asia, surveys for, and exchanges of natural enemies were carried out in the USSR 
and China, the native areas of many introduced U.S. weeds (Coulson 1981a; Coulson et al. 1982); 
beginning in 1988, as a result of new agreements between the U.S. and the USSR and PRC (see 
section B.1.a above), increased field studies in these areas were conducted by personnel of the ARS 
laboratories in Italy and South Korea (Fornasari and Pemberton 1993), Australia (Balciunas and 
Chen 1993), Frederick, MD, Bozeman, MT, Gainesville, FL, and Temple, TX, and have included 
surveys for weed pathogens (see section C.1, below). 


The first exploration in China was actually conducted in 1987, targeting leafy spurge (Fornasari and 
Pemberton 1993), and biological control of weeds research was soon begun at the Asian Parasite 
Laboratory (APL) in South Korea with work on Tamarix spp. (1991) and "water caltrop" (or water- 
chestnut) (1992). This work was terminated upon closing of the APL in 1993. 


re 


During 1973-85, the research program of the Biological Control of Weeds Research Laboratory at 
Albany, CA, shifted from programs on aquatic weeds (i.e., alligatorweed and waterhyacinth) and 
back to research on biological control of rangeland weeds, including tansy ragwort (1959-78), Scotch 
broom (1960-75), puncturevine (1961-65, 1976-80), halogeton (1964-66, 1975), alligatorweed 
(1964-74), Mediterranean sage (1966-76), Russian thistle (1968-80), milk and Italian thistles 
(1969-78), spotted and diffuse knapweeds (1973-87), rush skeletonweed (1974-82), leafy spurge 
(1974-87), and yellow starthistle (1976-78, 1982-present). New personnel (S. S. Rosenthal and R. W. 
Pemberton) joined the Albany staff in 1980-81 to replace persons retiring (R. B. Hawkes) or 
transferring (P. H. Dunn). A plant pathologist (J. M. Klisiewizc, ARS-Davis, CA) was assigned to the 
program during 1981-86 and conducted studies of indigenous pathogens of yellow starthistle and 
common purslane. Botanist C. E. Turner was added to the staff in 1984; S. L. Clement joined the 
staff briefly in the early 1980s, but transferred to the Rome laboratory. Some of the research by 
personnel of the California laboratory during this period has been reported in the following papers: 
Hawkes and Mayfield 1976; Andres 1978; Dunn 1978; Hawkes and Johnson 1978; Sobhian and 
Andres 1978; Maddox and Andres 1979; Maddox 1982; Klisiewicz et al. 1983; Klisiewicz 1985; 
Rosenthal 1985; Pemberton 1986; Maddox and Sobhian 1987; DeLoach 1991a; Rosenthal et al. 
1994; and 12 papers by ARS and university colleagues on 12 target rangeland weeds in Nechols et al. 
1995. (See also references cited in the section on significant accomplishments, below.) 


A new, expanded research quarantine facility for the laboratory was designed and constructed 
specifically for biological control, and the unit moved into new quarters at the Western Regional 
Research Center at Albany in 1986. In 1985, the biological control of weeds research unit was 
administratively shifted from the office of the ARS CA-NV-HI Area Director in Fresno, CA, to the 
Western Regional Research Center at Albany, where the unit became one of several "projects" under 
the Center's Plant Protection Research Unit following a Center reconsolidation program. L. A. 
Andres served as Research Leader of the biological control unit at Albany from 1964 until the 1985 
consolidation, at which time he became Project Leader until his retirement in September, 1988. C. E. 
Turner served as Project Leader from 1988 to present. As a result of reviews of the biological control 
of weeds program in 1985-86, decisions were made by the National Program Staff (in the absence of 
a NPL for biological control) that resulted in the downgrading of the spurge and knapweed projects 
at Albany and the reassignment of these projects, plus three biological control scientists, from 
Albany to Bozeman, MT, in 1987, to emphasize introduction and evaluation studies on the control of 
these weeds, both of importance to that area. The newly constructed non-quarantine plant growth 
facilities, which had been designed for biological control research, were temporarily released to 
other, biotechnologically-oriented research at Albany. Montana State University at Bozeman was in 
the process of strengthening its biological control of weeds program and new quarantine facilities 
were constructed by the university at Bozeman to accomodate the transferred ARS personnel as well 
as university needs. The quarantine facility became operational during 1988; see additional 
comments on the ARS Bozeman location below. Also, the APHIS-PPQ biological control 
implementation program initiated a biological control of weeds project on leafy spurge and 
knapweeds, and stationed several persons at the Bozeman location; see Chapter VI. Following 
several retirements, only one ARS scientist (C. E. Turner) remained at Albany by 1988 to continue 
biological control research on yellow starthistle and other weeds. In 1989, a second scientist (B. D. 
Perkins) was added to the Albany facility (though administratively under the ARS Bozeman 
laboratory) for testing and release of agents on gorse and Dalmatian toadflax, but he retired in 1992. 
During 1988-90, the Albany quarantine facility was shared with APHIS-PPQ biological control 


personnel importing natural enemies of leafy spurge provided by the ARS laboratory in Rome and 
other cooperators. 


The research program on rangeland weeds formerly headed and coordinated by the Albany unit from 
1958-87 involved many ARS and state cooperators in many western states (Andres and Kok 1981): 
ARS cooperators were located at ARS facilities at BCIRL, Columbia, MO; BIIL, Beltsville, MD; the 


78 


Forage and Range Research Unit, Lincoln, NE; and the Rangeland Insect Laboratory, Bozeman, MT 
(Puttler et al. 1978; McCarty and Lamp 1982; Rees 1977, 1982; and the section below on BIIL). The 
ARS Aquatic Weed Control Research Laboratory at Davis, CA, also cooperated with the Albany 
laboratory in the release of waterhyacinth bioagents in California. ARS cooperators with the current 
program remain at all locations except Beltsville, MD. 


The new ARS biological control of weeds unit, the Rangeland Weeds Laboratory at Bozeman, MT, 
with its access to Montana State University quarantine facilities, and the APHIS-PPQ biological 
control program, assumed the role of coordinating activities in regard to the rangeland weeds of the 
northern states. Of the three ARS scientists reassigned to Bozeman from Albany in 1987, one retired 
(D. M. Maddox) and one (R. W. Pemberton) was later reassigned to the Asian Parasite Laboratory 
(see section B.1.a). The latter was replaced by P. C. Quimby, who transferred from Stoneville in 
1989 to serve as Research Leader for the newly designated ARS Rangeland Weeds Laboratory at 
Bozeman. The biological control of weeds group at Bozeman consisted of S. S. Rosenthal (who 
retired in 1993) and N. E. Rees (who transferred to the unit from the ARS Rangeland Insect 
Laboratory at Bozeman, where he had conducted release studies of introduced insects on thistles and 
leafy spurge). A plant pathologist, A. J. Caesar, was added to the unit in 1991 (see section C.2 
below). Satellite locations were established at Sidney, MT (see below), and Albany, CA (for gorse 
and Dalmatian toadflax research; see above). Research directed from the Bozeman location focused 
primarily on study and release of introduced natural enemies of leafy and cypress spurges and 
spotted, diffuse and squarrose knapweeds, in cooperation with scientists of Montana State 
University, and other western universities, and with Canadian and APHIS biological control of weeds 
programs. Coordination between the two latter programs and the ARS program, initially a problem, 
has improved significantly since the ARS Research Leader position at Bozeman was filled in 1989. 
Much of the ARS research has been funded in part by USDI's Bureau of Land Management and 
Bureau of Indian Affairs. Some of the resulting research at Bozeman dealing with introduced 
invertebrates (including a nematode, Subanguina picridis, for Russian knapweed) is reported in the 
following papers: Rees 1990, 1991 (thistles); Pemberton and Rees 1990, Rees and Spencer 1991, and 
Rees 1992 (spurges); Rees and Story 1991, Rosenthal et al. 1991, and Rosenthal and Piper 1995 
(knapweeds); Quimby et al. 1991 and DeLoach 1991a (general); and Caesar (T.) et al. 1993 
(nematode). 


An additional ARS unit joined the rangeland weed program, with the transfer in 1987 of N. R. 
Spencer from Stoneville, MS, to conduct biological control research at the ARS Northern Plains Soil 
and Water Management Research Laboratory, Sidney, MT, under the technical supervision of the 
Bozeman laboratory. Studies at Sidney have concentrated on the collection of introduced natural 
enemies of leafy spurge and Canada thistle from their U.S. and Canadian areas of establishment and 
their recolonization in North Dakota and eastern Montana. 


During 1973-93, research iological contr i continued at the old IIPI locations at 
Gainesville and Fort Lauderdale, FL (see Chapter III, section B). ARS researchers at the Gainesville 
quarantine facility have been N. R. Spencer (1970-77) and G. R. Buckingham (1977-present). The 
research at this location during this period has been on imported natural enemies of alligatorweed 
(1973-74, 1979-80), waterhyacinth (1973-84), Eurasian watermilfoil (1974-present), hydrilla 
(1976-present), and melaleuca (1992-present). In addition, research on waterlettuce (1986-90) was 
conducted at this facility by D. H. Habeck (University of Florida) under a cooperative agreement 
with the ARS Fort Lauderdale laboratory. Much of this research, including overseas surveys, was 
made possible via cooperative agreements between the ARS Fort Lauderdale laboratory and the 
University of Florida (J. K. Balciunas, now with ARS), and was supported by the U.S. Army Corps 
of Engineers and the former Florida Department of Natural Resources (consolidated with the Florida 
Department of Environmental Regulation in 1992 to become the Florida Department of 
Environmental Protection). Quarantine service activities in regard to introduced insect parasites also 


719 


was conducted at Gainesville, until 1973 (see section B.1.a). The Gainesville location was 
administratively linked with the Fort Lauderdale laboratory beginning in 1985. (Spencer 1973; 
Spencer and Lekic 1974; Spencer and Coulson 1976; Center and Spencer 1981; Buckingham and 
Ross 1981; Buckingham and Bennett 1981, 1989; Buckingham and Buckingham 1981; Buckingham 
et al. 1983a, 1989, 1992; Buckingham 1984, 1988, 1994; Balciunas and Minno 1985; Bennett and 
Buckingham 1991; Balciunas and Purcell 1991.) 


The biological control of aquatic weeds program benefited greatly from the special foreign currency 
program (PL-480) during the 1960s and 1970s. This program provided foreign exploration for 
biological control agents of waterhyacinth in Uruguay, hydrilla in Pakistan, Eurasian watermilfoil in 
Yugoslavia, and several weed species in India. (Silveira-Guido 1965; Ghani 1976; Rao and Sankaran 
1974; and Lekic and Mihajlovic 1970.) 


Biological control of aquatic weeds research initiated by IIPI in 1972 at the ARS Aquatic Plant 
Management Laboratory at Fort Lauderdale has been directed by B. D. Perkins (1972-76) and T. D. 
Center (1978-present). This research has been supported by the Aquatic Plant Control Research 
Program and the Jacksonville District of the U.S. Army Corps of Engineers, the Florida Department 
of Environmental Protection, the Southwest Florida Water Management District, and the National 
Park Service of the U.S. Department of the Interior. Studies there have consisted of release and field 
evaluations of imported natural enemies of alligatorweed, waterhyacinth, hydrilla, and waterlettuce, 
following quarantine research and clearance procedures conducted first at the Albany quarantine 
facility and, from 1977, at the Gainesville location. A hiatus in natural enemy introductions occurred 
in the aquatic weed program from 1977 until the first releases of natural enemies of hydrilla and 
waterlettuce in 1987. This was due to the lack of a coordinated foreign exploration program between 
1974 and 1982, and unresolved questions on the specificity of agents for submersed weeds. This 
program gap was filled by the development of a cooperative agreement with the University of Florida 
in 1981. This agreement provided a university research associate position, subsequently filled by 

J. K. Balciunas, that was intended specifically for foreign exploration for biological control agents 
for hydrilla. Several new weeds are targeted for research at Fort Lauderdale, including the wetland 
tree melaleuca, for which research on natural enemies was initiated at the new Australian laboratory 
in 1988 (see this section above). (Center and Durden 1981, 1986; Balciunas and Center 1981, 1991; 
Center et al. 1982a, 1982b, 1990; Center 1982a, 1984, 1987, 1992a, 1994; Haag and Center 1988; 
Dray et al. 1990, 1993; Center and Kipker 1991; Center and Wright 1991; Center and Dray 1992; 
Dray and Center 1992 a and b.) 


The results of much of the research on biological control of aquatic weeds conducted at both 
Gainesville and Fort Lauderdale are contained in many of the reports and miscellaneous papers of the 
U.S. Army Corps of Engineers' Aquatic Plant Control Research Program published by the Corps' 
Waterways Experiment Station, Vicksburg, MS. (Pemberton 1980; Buckingham et al. 1981; Center 
1981, 1982b, 1983, 1992b; Center and Durden 1984; Center et al. 1984; Balciunas and Minno 1984; 
Balciunas 1985; Markham 1986; Dray et al. 1988; Center and Dray 1991; Dray and Center 1992 a 
and b; Buckingham and Okrah 1993.) 


Research on the biological control of aquatic weeds has also been conducted at the ARS Aquatic 
Weed Control Research Laboratory at Davis, CA. Research on competitive plants and the diploid 
grass carp (Ctenopharyngodon idella) initiated in the early 1970s by R. Yeo was resumed during the 
mid-1980s, the latter by L. W. J. Anderson and R. T. Pine, focusing on the sterile triploid fish. The 
Davis laboratory collaborated with the Corps of Engineers and the California Department of Food 
and Agriculture (CDFA) on the release of waterhyacinth insects in the Sacramento Delta. The 
quarantine facility at Albany, CA, under the direction of L. A. Andres, also collaborated in this 
effort. In 1990, the Davis laboratory, under the direction of L. W. J. Anderson and enabled with 
funding from CDFA, began an effort to establish the "hydrilla weevil" Bagous affinis in California. 


80 


Plans include similar effort with the "hydrilla leaf-mining fly" Hydrellia pakistanae. Quarantine and 
field evaluation support for these studies is being provided by C. E. Turner of the Albany laboratory. 
(Yeo and Holm 1981; Stewart et al. 1988; and Pine and Anderson 1989, 1991.) 


Two new ARS biological control of weeds units, planned prior to 1973 by IIPI, and both with 
associated quarantine facilities (Bailey and Kreasky 1978; Boldt 1982), were established during this 
period. The one located at the ie Whi arch Center neville, MS, initially 
focused on the study of the arthropod fauna of narcotic plants, under the leadership of J. C. Bailey 
(1972-77), in association with the research at the ARS laboratory at Rome (see above). The 
Quarantine Laboratory for Plant-Feeding Insects at Stoneville was constructed specifically for the 
quarantine testing and production of narcotic plant-feeding arthropods, and for use as a biological 
control of weeds quarantine receiving center after cessation of the narcotics program (Bailey and 
Kreasky 1978). Following the closing of the narcotics program in 1977, the quarantine facilities 
became the Stoneville Research Quarantine Facility (SRQF), first under the ARS Southern Weed 
Science Laboratory (SWSL) and later transferred to the Bioenvironmental Insect Control Laboratory 
(later the Southern Field Crop Insects Management Laboratory [SFCIML] and now Southern Insect 
Management Laboratory [SIML]) at Stoneville. The facility was used extensively for quarantine 
receipt of insect parasites and predators (see section B.1.a), and to a lesser extent by research 
workers assigned to the SWSL at Stoneville (Jones et al. 1985). Studies on the biological control of 
pasture, row crop, and aquatic weeds of the Southeast by use of arthropods at the SWSL from 1972- 
86, and subsequent research on pathogens, were conducted under SWSL Directors C. R. Swanson 
(until 1974), C. G. McWhorter (1974-87), and S. O. Duke (1987-present). Leaders of the biological 
control research unit (combined with the weed management research unit in 1987) within the SWSL 
were K. E. Frick (1972-77), P. C. Quimby (1978-87), and G. H. Egley (1987-93). Biological control 
research, which actually began in 1971 with the transfer of Frick from California to Stoneville that 
year by IIPI, included: study of imported and/or native insect enemies of puncturevine, velvetleaf, 
and curly dock by Frick, Quimby (from 1972), and N. R. Spencer (from 1982); study of the potential 
control of purple nutsedge by augmentation of the native moth Bactra verutana by Frick, Quimby 
and J. M. Chandler (1971-81); and study of the impact of natural enemies of alligatorweed and 
waterhyacinth by G. B. Vogt and Quimby (1973-86). A research program on control of weeds by use 
of indigenous weed pathogens was initiated by the SWSL in 1973 (see section C.2, below), and after 
the retirements of Vogt and Frick and transfer of Spencer to the SFCIML in 1986, research on the use 
of arthropods for weed control was phased out. Biological control of weeds research at Stoneville is 
now focused on use of indigenous pathogens. (Frick and Garcia 1975; Garcia and Frick 1975; 
Spencer 1984, 1988, 1990; Vogt et al. 1979, 1992.) 


Research at the second ARS biological control laboratory planned by IIPI prior to 1973, is located at 
the Grassland, Soil and Water Research Laboratory at Temple, TX. The research has been directed 
by C. J. DeLoach since his return from the Argentine laboratory in 1974, and with the addition of 

P. E. Boldt after his return from the Rome laboratory in 1982. Research at Temple has addressed 
biological control of native and introduced weeds and brush of the southwestern rangelands by the 
introduction of foreign control agents. The emphasis on native weeds was because of the ca. 20 
southwestern rangeland weeds and brush with biological control potential, of which all but two are 
native. This has been the only project anywhere in the world devoted to classical biological control 
of native weeds in a continental area. 


Native weeds investigated have been honey mesquite, broom and threadleaf snakeweeds, common 
and "Texas” broomweed, creosotebush, seepwillow and other Baccharis spp., Texas whitebrush, 
bitter rubberweed, "tarbush", and others, all of which have related species native in Argentina, and 
for which close ties with the Argentine laboratory were essential (DeLoach 1981a). All of these 
native plants, which occurred in restricted areas or at low or moderate densities when European 
settlers first arrrived, have increased enormously in density during the last 150 years, and now cause 


81 


serious losses in rangelands over wide areas of the Southwest. Two projects were also initiated to 
control native plants that are primary pests of crops and secondarily of pastures and ranges; these 
were common cocklebur and hemp sesbania. Conflicts of interest over the harmfulness versus 
benefits of these targeted weeds have been addressed, and approval was granted by the TAG to 
proceed with biological control projects for snakeweeds and broomweeds, seepwillow, whitebrush 
and bitter rubberweed, provided that suitable natural enemies could be found. 


Much has been accomplished in the development of theory and application that demonstrates that 
biological control of native weeds is both possible and feasible if the target weeds and biological 
control agents are carefully selected (DeLoach 1978, 1981). Much information has been obtained on 
the host range, ecology, life history and impact of native U.S. natural enemies of the target weeds, 
and of South American natural enemies of related species, regarding the following: 1) honey 
mesquite (DeLoach 1981b, 1982, 1983 a and b; Cordo and DeLoach 1987; Cuda et al. 1990), which 
was eventually discarded as a target because of significant beneficial qualities (DeLoach 1986); 2) 
snakeweeds and broomweeds (Foster et al. 1981; DeLoach and Psencik 1982 a and b; DeLoach, 
1991b; Cordo and DeLoach, 1992), for which studies in Temple quarantine of two Argentine species 
were conducted, one of which, a weevil (Heilipodus ventralis), was released in Texas; 3) Baccharis 
spp. (Boldt 1987, 1989 a, b and c; Boldt and Robbins 1987, 1990, 1992; Boldt et al. 1988, 1991; 
Gagné and Boldt 1989; Boldt and White 1992; Boldt and Staines 1993), for which two insects were 
tested in quarantine at Temple, but neither was released, and Baccharis spp. have been discarded as 
targets, at least temporarily; and 4) creosotebush (Cordo and DeLoach 1993). 


In practice, control has not yet been achieved for any of the target native weeds. The primary 
difficulties have been 1) conflicts of interest for certain weeds (the weed has substantial beneficial 
values), 2) few insects overseas that are sufficiently host specific, and 3) the overseas insects do not 
feed and develop well on certain of the target U.S. weed species. 


Only a few introduced weeds are of much importance in southwestern rangelands. The most 
important of these is saltcedar, although Russian-olive is rapidly invading riparian sites in more 
northern areas, and the poisonous African rue, which occurs sporadically, is spreading along 
highways. 


Saltcedar, first proposed as a candidate for biological control in the early 1970s by L. A. Andres, was 
studied under PL480 programs in Pakistan and Israel, during which numerous promising candidate 
insects in both areas were identified. However, further research was postponed until there could be a 
resolution of the conflicting economic interests concerning this weed. Beginning in 1987, an 
extensive review of the literature and analysis of the harmful and beneficial values of saltcedar and 
of its potential for biological control was conducted at Temple, and the resulting petition to the TAG 
in 1989 resulted in the resolution of the conflict and allowed the testing of insects for introduction to 
begin. Additional surveys for natural enemies have recently been conducted by ARS European 
laboratory scientists in southern Europe and North Africa and in the People's Republic of China and 
by the Asian Parasite Laboratory in 1991. More extensive surveys were conducted there by C. J. 
DeLoach and staff of the Sino-American Biological Control Laboratory (SABCL) in 1992-93. 
Preliminary surveys began in Turkmenistan during the summer of 1993 by EBCL scientists. Host 
range testing of candidate agents began in 1991 by EBCL and Israeli cooperators, and two insect 
species are currently undergoing quarantine testing at Temple. See DeLoach 1990. 


Also, follow up studies on projects to control introduced weeds initiated by other ARS laboratories 
have been undertaken at Temple, to establish those natural enemies in Texas that already were tested 
overseas or in some cases already released and established in other areas of the U.S. These projects 
included Russian thistle, milk and musk thistles (Boldt and DeLoach 1986, and Boldt and Jackman 
1993), and field bindweed (Ciomperlik et al. 1992, and Boldt and Sobhian 1993). Natural enemies of 


82 


these weeds were established in Texas, and the introduced mite Aceria malherbe appears to be 
dispersing and shows promise of substantially reducing the growth of field bindweed. 


In 1974, research on biological control of weeds was initiated by the Beneficial Insect Intr. 
Laboratory (BIL), at Beltsville, MD, with the hiring of S. W. T. Batra, in order to take advantage of 
previous research and the clearance and release of insect enemies of weeds elsewhere in the U.S. 
against weeds also common in the northeastern region. Investigation of the potential for the 
biological control of other weeds of northeastern pastures was also initiated. The BIIL (later BIL, see 
section B.1.a) biological control of weeds research program was hampered by the lack of nearby 
quarantine facilities. Nevertheless, natural enemies of thistles, knapweeds, and spurges, provided by 
the Albany laboratory, state cooperators, and Canadian sources, were established in the Northeast. A 
number of northeastern pasture weeds were identified as having potential for classical biological 
control, including bedstraws, hawkweeds, smallflower galinsoga, and others; see Batra 1979, 1980, 
1981, 1983, 1984. Unfortunately, economic data sufficient to justify a sustained biological control 
program at the ARS laboratory in Rome was not obtained for any of the potential targets (see 
discussion above concerning establishing priorities). As a result of BIIL's initial research efforts on 
Carduus and other thistles, funded in part by the Maryland Department of Transportation, the 
Maryland Department of Agriculture later instituted a biological control of weeds program, with 
emphasis on thistles, and in 1989 established a quarantine facility at Annapolis (Tipping and Hight 
1989). The last targeted weed for the BIL program was purple loosestrife (Batra et al. 1986; Hight 
1990; Kok et al. 1992 a and b; Malecki et al. 1993); overseas and quarantine research on the 
biological control of this wetland weed was funded by the U.S. Fish and Wildlife Service; the 
overseas studies were conducted under contract by the International Institute of Biological Control 
(IIBC) and the quarantine studies by VPI scientists. Three European beetles (Hylobius 
transversovittatus, Galerucella calmariensis, and G. pusilla) were imported and released in 1992 in 
several sites throughout the U.S., and in Canada, and at least two were found to have overwintered 
and begun oviposition in 1993 (Malecki et al. 1993). The biological control of weeds program in the 
northeastern region lost much of its funding with the departure in 1985 of the research scientist 
(Batra) assigned to the program (studies continued by the support scientist S. D. Hight), and was 
never thereafter adequately supported by ARS. Consequently, the program was terminated by the 
National Program Staff at the end of Fiscal Year 1993. 


During this period, ARS also contracted with university workers in Virginia (VPI) to speed clearance 
of insects attacking musk and related thistles (see also Chapter III, section B and section B.1.a of this 
Chapter), and at the University of Idaho to facilitate the development of an integrated pest 
management program against yellow starthistle utilizing chemicals, plant competition, and biological 
control strategies. The successful VPI program led to the redistribution of two introduced musk 
thistle natural enemies that became established in Virginia, and as such provided reciprocal support 
for the ARS thistle program at Beltsville, MD. 





weeds as ng 1973-93 elds 7 seRedictict a SabanatRt of 33 new exotic Weed: ‘feeding 
invertebrates (including a nematode) into the United States, only some of which are listed by Julien 
(1992). Several of these projects have resulted in control of the weeds in portions of their ranges. 
(Two foreign pathogens were also established during this period; see section C.2 below for 
accomplishments of the ARS programs utilizing foreign and endemic pathogens for control of 
weeds.) 


Evaluation of the tansy ragwort program was conducted during the period. The dramatic control of 
tansy ragwort, a poisonous pasture and range weed, throughout its range in California, Oregon, and 
parts of Washington matched the levels of control achieved in the early common St.-Johnswort 
program. The improved control was primarily due to the feeding of an earlier introduced small 


83 


chrysomelid beetle, Longitarsus jacobaeae, that attacks the leaves, crowns, and roots of the plant 
(Hawkes and Johnson 1978; Pemberton and Turner 1990). See also the discussion of the economic 
results of this program in Chapter III, section B. The Oregon Department of Agriculture has been 
instrumental in distributing the introduced ragwort insects throughout the state to the extent that they 
now pay some farmers to maintain ragwort to serve as a source of future beetle collections. This 
project demonstrated the need for such distribution programs, leading to the development of such a 
program in APHIS; see Chapter VI. The Colorado and New Jersey Departments of Agriculture have 
been similarly involved in distributing introduced weed natural enemies, for thistles and other weeds, 
in their states. 


Rush skeletonweed, a tough-stemmed composite that has the potential to spread into grain areas of 
the West and reduce production as well as hamper harvesting, has been curbed by the introduced rust 
(Puccinia chondrillina), leaf- and stem-galling midge (Cystiphora schmidti), and stem-tip-galling 
eriophyid mite (Eriophyes chondrillae). The rust has reduced stem height in California, while the 
eriophyid mite has been credited with reducing plant abundance in Washington (Piper 1986). 


Eleven new agents have been introduced against leafy spurge, a weed toxic to cattle in the northern 
great plains, 12 against diffuse and spotted knapweed, one (a nematode) against Russian knapweed in 
the northern and northwestern states, and five species against yellow starthistle in the West and 
Northwest. At least five insect species have been established on the aquatic weeds waterhyacinth, 
waterlettuce, and hydrilla (discussed below). And at least two, and probably three, European species 
of beetles are provisionally established on purple loosestrife in the Northeast. Some of these natural 
enemies have not had time to fully demonstrate their control potential. 


Yellow starthistle is an annual weed from southern Eurasia that is highly invasive on rangelands and 
other environments in the far western states. The weed displaces native plants, is poisonous to 
horses, and the spiny heads deter grazing by cattle as well as human enjoyment of infested 
recreational lands. Early work by ARS and the University of California, initiated in 1959 and the 
early 1960s, did not directly result in the establishment of any biological control agents. The yellow 
starthistle project was rejuvenated in the 1980s when ARS made it a high priority project at the 
Albany and Rome laboratories. R. Sobhian was stationed in Greece for work on this weed, and D. M. 
Maddox from the Albany laboratory went to Greece one summer to help run a field-plot, host- 
specificity experiment on Bangasternus spp. Progress has been very rapid since then, thanks in great 
part to simultaneous host-specificity experiments carried out in the field in Greece by Sobhian and 
others, at the Rome laboratory by S. L. Clement and L. Fornasari, and at the Albany laboratory by D. 
M. Maddox and C. E. Turner. Since the mid-1980s, five insects have been introduced from Greece 
and have successfully established in the U.S.: the tephritid flies Urophora sirunaseva and 
Chaetorellia australis, and the weevils Bangasternus orientalis, Eustenopus villosus, and Larinus 
curtus. All five species attack the flowerheads and reduce seed production, the only means of 
reproduction by this weed. These insect species feed on different parts of the flowerhead and attack 
the heads at different stages of development. Among the five species, the flowerhead is attacked at 
all stages of development, from the earliest closed bud stage to full flowering. It is too soon to know 
the impact of these insects, but they almost certainly should slow the rate of invasiveness of the weed 
over the short and long term. (Maddox and Mayfield 1985; Maddox et al. 1985, 1990; Sobhian and 
Zwilfer 1985; Maddox and Sobhian 1987; Clement 1990, 1994; Groppe et al. 1990; Clement and 
Sobhian 1991; Fornasari et al. 1991; Sobhian 1993b; Turner 1994; Turner et al. 1994, 1995; 
Fornasari and Turner 1995.) 


Leafy spurge is an extensively rooted perennial herb from Eurasia that is weedy on rangelands in the 
northcentral states and adjacent areas of Canada. The weed can dominate rangeland vegetation, and 
produces a latex that causes dermatitis in cattle and humans. A biological control program against 
spurges was initiated by Agriculture Canada and CIBC/IIBC in the 1960s. ARS joined this research 


84 


effort in the 1970s through work carried on at the Albany (P. H. Dunn, R. W. Pemberton) and Rome 
(P. H. Dunn, P. Pecora) laboratories. The domestic program shifted to Bozeman with the transfer 
there of R. W. Pemberton from Albany in 1987. APHIS has carried out a high level of 
implementation activity on this weed since the late 1980s. 


A total of 11 insects has been imported from Eurasia and released in the U.S. against leafy spurge. 
Establishment is confirmed for eight of these. These insects and the years of their first U.S. release 
are as follows: the hawk moth Hyles euphorbiae (1964), the clearwing moth Chamaesphecia 
tenthrediniformis (1975), the long-horned beetle Oberea erythrocephala (1980), the gall midge 
Spurgia esulae (1985), the flea beetles Aphthona flava (1985), A. cyparissiae (1986), A. czwalinae 
(1987), A. nigriscutis (1989), A. abdominalis (1993), and A. lacertosa (1993; an accidental release of 
this species was apparently made in 1988), and the clearwing moth Chamaesphecia hungarica 
(1993). Through 1993, establishment is confirmed for all but C. tenthrediniformis and the two insects 
first officially released in 1993. In terms of specific research efforts by ARS, the agency has carried 
out U.S. releases of all these insects except the second clearwing moth, C. hungarica. ARS has 
performed the host specificity studies on four of the Aphthona species and S. esulae, as well as on the 
gall midge Dasineura sp. nr. capsulae, and the moths Oxicesta geographica, Simyra dentinosa, and 
Chamaesphecia crassicornis. 


The most promising biological control agents for leafy spurge appear to be the Aphthona flea beetles, 
due to their relatively high level of host specificity and effectiveness. Most of the damage is done by 
the larvae, which feed on the roots of the weed. Substantial reductions of leafy spurge are becoming 
evident in areas following the release of these flea beetles, especially with A. flava and A. nigriscutis. 
Following his transfer to the Asian Parasite Laboratory in 1989, R. W. Pemberton discovered 
Aphthona flea beetles on leafy spurge in China (Inner Mongolia). Two of these Chinese species, A. 
chinchihi and A. seriata, have undergone host-specificity assessment in Europe and Bozeman, MT. 
(Dunn 1979; Pemberton 1986; Rees et al. 1986; Pemberton and Wang 1989; Pemberton and Rees 
1990; Pemberton 1995.) 


Diffuse knapweed and spotted knapweed are biennial and perennial herbs, respectively, that are 
native to Eurasia and weedy on rangelands in the northwestern United States and southwestern 
Canada. Historically, biological control research on these weeds was begun in 1961 by Canada and 
CIBC/IIBC, and their strong activity on these weeds has been ongoing. Since the late 1980s, Montana 
State University has had a high level of domestic activity on knapweéds, particularly spotted 
knapweed. Since the late 1980s, APHIS has carried out a high level of implementation work on 
knapweed insects. ARS has contributed a greater research effort to diffuse knapweed than to spotted 
knapweed. The biological control agents released have been European insects that attack the heads or 
roots of knapweeds. A total of 12 insects have been intentionally introduced into the United States 
against these two knapweeds, and another species spontaneously colonized the United States from 
Canada. Of these 13 knapweed insects, ten are confirmed established through 1993. Some of these 
insects attack both knapweed species, while others preferentially attack one or the other knapweed. 
Some of these knapweed insects also attack another weedy knapweed, squarrose knapweed. The 
earlier ARS research was done by the Albany laboratory (D. M. Maddox, S. S. Rosenthal) and the 
Rome lab (P. H. Dunn, R. Sobhian), with the domestic effort transferring to the Bozeman laboratory 
with the transfer of S. S. Rosenthal there in 1987. As there have been many recent releases of new 
agents, it is too soon to know their control impact. However, due to the combined impact of head and 
root insects, the biological control potential appears to be excellent. 


The knapweed insects and the years of their first releases into the U.S. are as follows: the fly 
Urophora affinis (1973), the moth Metzneria paucipunctella (1980), the beetle Sphenoptera 
jugoslavica (1980), the moths Agapeta zoegana (1984), Pelochrista medullana (1984), and 
Pterolonche inspersa (1986), the weevils Cyphocleonus achates (1988), Bangasternus fausti (1989), 


85 


and Larinus minutus (1991), the flies Chaetorellia acrolophi and Terellia virens (1992), and the 
weevil Larinus obtusus (1993). The fly Urophora quadrifasciata spontaneously spread to the U.S. 
from Canada in 1980. Establishment is confirmed for all of these except P. medullana, P. inspersa, 
and L. obtusus. ARS has specifically performed host specificity studies on P. inspersa, B. fausti, L. 
minutus, and U. quadrifasciata; and has carried out field releases of most of the others listed. 
(Maddox 1982; Maddox and Sobhian 1987; Dunn et al. 1989; Groppe et al. 1990; Rees and Story 
1991; Sobhian et al. 1992a; Piper and Rosenthal 1995; Story 1995.) 


Though much basic information has been gathered in connection with the unique research program at 
Temple, TX, on native weeds and brush of southwestern rangelands (see discussion above), which 
has been a difficult and controversial program because of major conflicts of interest, control has not 
yet been achieved for any of the targeted native species. Only one foreign natural enemy has been 
released in the U.S. to date, the weevil Heilipodus ventralis against snakeweeds, but it has so far 
failed to establish. Research on introduced weeds in Texas has resulted in the establishment of a 
promising natural enemy of field bindweed, as a result of previous research by the Albany laboratory 
(Rosenthal and Platts 1990). And prospects for control of saltcedar are promising. See discussion of 
the Texas program above. 


Waterhyacinth, a floating aquatic weed that covers the surface of lakes and slowly moving water, has 
been reduced to one-third of its former abundance in the Gulf Coast states (Cofrancesco et al. 1986; 
Center et al. 1990). This reduction has resulted not from removal of biomass by introduced insects, 
but rather reduced regrowth following annual winter die-back. Two weevils and a moth introduced 
from Argentina (1972-77) tunnel the leaf petioles and plant crown, destroying meristematic tissue in 
the process. Having lost the ability to replace senescent tissue as a result of this damage, the plants 
sometimes lose bouyance and sink. More often, they merely stop growing. In recent experiments, for 
example, standard-sized plots inoculated with the weevils expanded during the growing season to 
cover only two to three times the initial area, whereas uninoculated controls expanded nearly 
six-fold. Hence, the success of this project seems to stem from the regulation of plant growth rather 
than from the wholesale destruction of plant populations (Center et al. 1990). 


Two Asian natural enemies of hydrilla were released in 1987 in Florida -- an ephydrid fly, Hydrellia 
pakistanae, and a tuber weevil, Bagous affinis. The fly is now well established throughout the 
Southeast and has overwintered as far north as northern Alabama. Hydrilla beds have either partially 
or completely degenerated at several release sites, but cause and effect have not yet been proven. 
There are plans to release this fly in California in 1994. The weevil, which requires prolonged dry 
periods, failed to establish in Florida from lack of suitable habitat. Promising results have been 
obtained in California by K. E. Godfrey of the Davis laboratory, however, so this insect may prove 
useful in areas with pronounced dry summers. An Australian ephydrid fly, H. balciunasi, was 
released in Florida in 1989 and Texas in 1991. Although it initially seemed to establish at early 
release sites in Florida, populations failed to persist. This may be partially attributable to site 
invasions by expanding populations of H. pakistanae. The releases in Texas by the U.S. Army Corps 
of Engineers (USACE) resulted in establishment of at least one population, which has grown and 
survived for over a year, despite the inadvertent release of H. pakistanae as a contaminant in the 
stock cultures. A stem weevil, Bagous hydrillae, also from Australia, was first released in Florida in 
1991, but establishment has not yet been verified. A strain of H. pakistanae from the north temperate 
region of China was first released in 1992, but may have been absorbed by the rapidly expanding 
populations of the Indian/Pakistani strains before a discrete population could establish. 


Under an ARS/University of Florida cooperative project on the biological control of waterlettuce 

sponsored by the USACE Jacksonville District, a South American weevil, Neohydronomus affinis, 
was obtained from the Australian Commonwealth Scientific and Industrial Research Organization 
(CSIRO), and released in 1987 in Florida. Although the weevil had been discovered and tested by 


86 


ARS scientists in Argentina (DeLoach et al. 1976), it was first successfully utilized as a biological 
control agent by the Australians. Complete control of waterlettuce was realized at two of three initial 
release sites within two years of the first release, and the species spread widely in Florida, both by 
natural dispersal and by means of a redistribution program by the Florida Department of Natural 
Resources (now Department of Environmental Protection). The USACE also released this species in 
Texas, and it has been found to be established in Louisiana (Grodowitz 1991). See also Thompson 
and Habeck 1989, and Dray et al. 1990. 


Some of the agents studied and introduced to the U.S. have also been exported to other countries. 
Consequently, successful efforts at biological control of waterhyacinth have been reported from the 
Sudan, India, Argentina, and Australia (Beshir and Bennett 1985; Jayanth 1987; DeLoach and Cordo 
1983; Wright 1981). Australia has also had good success with alligatorweed insects (Julien 1981). 


Much of the work in the rapidly expanding field of weed biological control is coordinated through an 
ongoing series of international symposia held quadriennially, and informal, annual meetings of 
European-stationed biological control of weeds specialists. The first of the symposia was held in 
1969 in Delémont, Switzerland, and was attended by 20 scientists from eight countries, resulting in a 
110-page published proceedings (Simmonds 1970). The sixth symposium was held in Vancouver, 
Canada, in 1984, and was attended by 135 scientists from 16 countries, and resulted in a 885-page 
published proceedings (Delfosse 1986). The seventh symposium was held in 1988, was attended by 
110 scientists, and was sponsored by the ARS laboratory in Rome and the Istituto Superiore di 
Santidad Vegetale (Delfosse 1990); the ARS laboratory had also sponsored the second symposium 
(Dunn 1973). The eighth symposium was held in Canterbury, New Zealand, in 1992, the proceedings 
of which (Delfosse & Hill, 1994) was not available by the end of 1993 for a comparison with the 
Vancouver and Rome symposia. 


Based on the difference in attendance between the 1969 and 1984/1988 symposia, there was an 
apparent 5- to 6-fold increase in the number of scientists addressing the biological control of weeds 
over those 20 years; this includes an increasing number of plant pathologists. Unfortunately, the 
number of ARS scientists addressing classical biological control of weeds by use of invertebrates has 
declined in recent years. In the early 1980s, about 19 ARS scientists were working full time in this 
field; today only 12 remain, and five are near retirement. 


2. Weed Pathogens. By W. L. Bruckart and J. R. Coulson 


Introduction. The period 1973-93 saw the organization of formal research on plant pathogens for 
biological control of weeds. Prior to this time, research in this area was tentative and random, 
without clear focus or major support (Wilson 1969). Research activities described in Wilson's paper 
and the success of entomologists in classical application of insects for weed control provided the 
necessary visibility and demonstrated potential to justify organization of a formal effort by the 
USDA-ARS in this area. Currently, plant pathogens are deployed in two ways. They can be 
introduced as classical agents like the foreign invertebrates, or they can be used like herbicides. 
Generally, the classical approach involves foreign pathogens for rangeland weed control and the 
bioherbicide approach involves endemic pathogens for control of weeds in row crops. Each of these 
approaches resulted from research prior to the period encompassed by this section. 


The earliest USDA involvement with a plant pathogen for biological weed control was sponsorship 
of R. I. Inman in 1965 by the ARS Crops Protection Research Branch to investigate the potential of 
the rust fungus, Uromyces rumicis, for control of curly dock (Inman 1971). This research was 
conducted in Rome, Italy, with a foreign pathogen intended for classical control of a U.S. weed. 
Results of this research were encouraging, but the pathogen has not been introduced into the U.S. to 
date, because U. rumicis is heteroecious and the host range determination with plants related to the 


87 


alternate host, "lesser celandine" (Ranunculus ficaria), was not accomplished until recently. This 
research initiated the concept of using foreign plant pathogens in a manner similar to the use of 
insects as classical biological control agents. 


The discovery of Colletotrichum gloeosporioides f. sp. aeschynomene (CGA) in 1969 at the 
University of Arkansas Rice Research and Extension Center initiated the concept that plant 
pathogens could be used in ways similar to herbicides, now known as the bioherbicide or 
mycoherbicide approach. Development of CGA involved cooperation between University of 
Arkansas and ARS (Stuttgart, AR) scientists (Daniel et al. 1973, 1974; Smith et al. 1973 a and b; 
Smith 1986). In 1974, CGA became the first pathogen patented for use as a mycoherbicide (Daniel et 
al. 1974), and in 1982 it was commercially registered for weed control (Bowers 1986; Smith 1986; 
Templeton 1988). 


Problems associated with 1) coordination of research activities (particularly in regard to a focused 
national program on classical biological control), 2) setting target weed priorities, and 3) conflicts of 
interest, that were described for development of insect biological control agents in the previous 
section (C.1 above), have also affected progress in development of plant pathogens as biological 
control agents. Also, regulations specific to microorganisms (and not to invertebrates) have been 
reevaluated by the Animal and Plant Health Inspection Service (APHIS) and Environmental 
Protection Agency (EPA) since 1973 because of the development and proposed use of plant 
pathogens for weed control; utilization of plant pathogens as weed control agents was slowed as a 
result of this review and reinterpretation of the regulations for microbes. 


Foreign pathogens. A research program on foreign pathogens for biological control of weeds was 
initiated in 1974 at the recommendation of the ARS Working Group on Natural Enemies of Insects, 
Weeds and Other Pests (WGNE). The ARS Plant Disease Research Laboratory (now the Foreign 
Disease-Weed Science Research Unit) at Frederick, MD, was designated for this effort. The 
Frederick Laboratory had an established facility designed for study of quarantine and containment of 
plant pathogens (Melching et al. 1983). This facility was designated as the ARS containment facility 
for receipt and study of exotic weed pathogens. ARS scientists involved in the biological control 
program at the Frederick facility have been R. G. Emge and C. H. Kingsolver (1974-80), W. L. 
Bruckart (1981-present), S. M. Yang (1987-present), A. R. Bennett (1987-1992), and D. G. Luster 
and N. W. Schaad (1993-present). 


The rust Puccinia chondrillina was the first foreign pathogen introduced into the United States for 
weed biological control. A strain of this fungus had been introduced previously from Europe into 
Australia for control of rush skeletonweed. Evaluation of European acquisitions of P. chondrillina 
were made in containment at Frederick in cooperation with Australian scientists at the 
Commonwealth Scientific and Industrial Research Organization's (CSIRO) laboratory in Montpellier, 
France (Emge et al. 1981). The pathogen was very host specific and aggressive on the most common 
form of rush skeletonweed in the U.S. Releases were made between 1976 and 1978 at locations in 
California, Idaho, Oregon, and Washington (Adams and Line 1984; Supkoff et al. 1988). The rust 
became established and spread throughout stands of susceptible biotypes of the target weed. In 
California, stand reduction varied from 55 to 87%, and P. chondrillina appeared to be the organism 
most damaging to rush skeletonweed over a 10-year period (Supkoff et al. 1985, 1988), which agreed 
with reports on the effects of the rust in Australia. 


Other fungi studied at the Frederick facility as candidates for biological control include the 
autoecious Uromyces spp., Alternaria spp. and Myrothecium verrucaria for leafy spurge control, 
Puccinia carduorum for Carduus thistle control, and Puccinia jaceae for control of Centaurea 
species (Bennett et al. 1991; Bruckart 1989; Shishkoff and Bruckart 1993; Yang et al. 1990, 1991, 
1993a). Nearly all risk assessment research on plant pathogens have been conducted in a containment 


88 


greenhouse at Frederick, unlike the study of invertebrate agents which involves preliminary 
investigations at overseas locations. Philosophy and protocols for development of these pathogens 
were modelled after those used by entomologists (Bruckart and Dowler 1986), but certain 
modifications have been incorporated that suit the development of plant pathogens (Bruckart and 
Shishkoff 1993). The primary reliance on greenhouse data for risk assessments necessitated 
incorporation of side-by-side greenhouse comparisons of candidate foreign pathogens with 
endogenous (endemic) fungi from North America for perspective about field performance (Bruckart 
and Shishkoff 1993). 


The most progress to date has been with Puccinia carduorum, a rust fungus proposed for use against 
musk thistle. Although pustules developed on some native North American thistles (Cirsium spp.) 
and artichokes under optimal greenhouse conditions for infection, reactions on non-target species 
were resistant and P. carduorum could not be maintained on these species, even in the greenhouse 
(Politis et al. 1984; Bruckart et al. 1985; Politis and Bruckart 1986; Bruckart and Shiskoff 1993). 
Phenotypic characterization using isozyme analysis and pathogen morphology related to differences 
between strains from different Carduus species noted in host plant inoculation studies (Bruckart and 
Peterson 1991). Similar results were found in field evaluations in Switzerland and Virginia (Baudoin 
et al. 1993; Bruckart et al. 1993). At the end of 1993, a proposal for general use of the pathogen in 
the U.S. was under review by APHIS and the U. S. Fish and Wildlife Service. 


Leafy spurge received considerable attention from plant pathologists during the period 1973-93. 
Collecting trips were made from the Frederick laboratory to Europe by S. K. Turner (1983, in 
cooperation with Montana State University) and A. R. Bennett (assigned to temporary summer duty 
at the ARS facilities in Italy and France between 1989-91). Also, G. Defago of the Institut fiir 
Spezielle Botanik in Switzerland, was funded by ARS between 1980 and 1985 to study the 
autoecious rust fungi in the genus Uromyces that attack leafy spurge (Defago et al. 1985). Additional 
trips to the former Soviet Union were made by A. J. Caesar (ARS, Bozeman, MT) in 1992 and 1993. 
Those explorations emphasized collection of soilborne pathogens, particularly Rhizoctonia spp., that 
may be related to a pathogen causing leafy spurge stand reductions in Montana (Caesar et al 1993b; 
Caesar 1994a). S. M. Yang made collecting trips to the People's Republic of China between 1989 and 
1993 as part of the Sino-American biological control collaborative program (Yang et al. 1991, 
1993a). Although leafy spurge has been the principle target, pathogens from Centaurea spp. 
(particularly yellow starthistle) and other thistles were sought. 


Endemi ens. Several contributions to the discovery, development, and evaluation of plant 
pathogens for use as mycoherbicides have been made through research at the ARS Southern Weed 
Science Laboratory in Stoneville, MS, begun in 1974. ARS plant pathologists at this location have 
been H. D. Ohr (1974-77), H. L. Walker (1974-85), and C. D. Boyette (1985-present). (See section 
C.1 above for other biological control of weeds research at Stoneville.) Among the fungi discovered 
and evaluated were A/ternaria cassiae from sicklepod, Fusarium lateritium from velvetleaf, A. 
crassa from jimsonweed, Colletotrichum truncatum from hemp sesbania, and A. helianthi from 
sunflower for common cocklebur (Walker 1980, 1981, 1982; Boyette and Walker 1985; Boyette 
1986, 1988, 1991 a and b; Quimby 1989; Boyette et al. 1991, 1993). Subsequent evaluation of A. 
cassiae was made on a regional basis through the S-136 Regional Research Committee and with 
involvement from federal, state, and private sectors (Charudattan et al 1986; Bannon 1988). The ARS 
contributions to the A. cassiae research also included development of procedures for 
mass-production and financial support for regional evaluation (Walker 1980, Walker and Riley 
1982). Commercial use of A. cassiae is pending EPA registration of a product through a commercial 
enterprise. 


Once a pathogen has been identified and found promising for application as a mycoherbicide, there 
are other, major hurdles to overcome in its development. The most significant of these obstacles are 


89 


scaling-up and formulation. ARS scientists have provided innovative advances in each of these areas 
that increases the potential for these pathogens to be utilized in weed management. Perspectives 
about both the process of and advances in mass production and formulation have been written by 
Quimby and Boyette (1987) and Daigle and Connick (1990). Innovations in carrier or formulation 
include the use of sodium alginate (Walker and Connick 1983), water-in-oil invert emulsions 
(Quimby et al. 1988; patented by Quimby 1990; later modified or improved by Boyette et al. 1993; 
Yang et al. 1993b), and a wheat gluten matrix called 'Pesta' (Connick et al. 1991, 1993). 


Recently, the expertise of scientists at the ARS Fermentation Biology Research Unit in Peoria, IL, 
was enlisted to investigate large-scale, liquid fermentation of fungi for use as mycoherbicides. 
Factors such as the C:N ratio in liquid media affects the yield and virulence of Colletotrichum 
truncatum conidiophores, and such must be considered in the large-scale, economic production of 
fungi for use in biological weed control (Schisler et al. 1991b, 1992; Jackson et al. 1992). Potential 
of Puccinia canaliculata, an obligate pathogen, as a mycoherbicide was evaluated at the Frederick 
location in cooperation with state and ARS scientists in Georgia and Maryland (Phatak et al. 1983; 
Bruckart et al. 1988). 


Study of endemic pathogens of leafy spurge and other rangeland weeds was initiated by A. J. Caesar 
and his colleagues at the Rangeland Weeds Laboratory in Bozeman, MT (Caesar 1994 a and b; 
Caesar et al. 1993 a and b). Caesar et al. (1993a) found a reduction in the density of rangeland weeds, 
and particularly leafy spurge, associated with "fairy ring-like" patches in the Montana rangelands. 
Pathogenic isolates of a Rhizoctonia sp. have been isolated from diseased leafy spurge in these areas 
(Caesar et al. 1993b; Caesar 1994a). 


Innovative research into use of endemic bacteria has been pursued by ARS scientists more recently. 
Crown gall, caused by Agrobacterium tumefaciens, was described recently on leafy spurge, Russian 
knapweed, and both spotted and diffuse knapweeds (Caesar 1994b). Rhizobacteria have been 
screened and field tested for potential to control downy brome and jointed goatgrass at Pullman, WA 
(Kennedy et al. 1991, 1992), and other weeds at Columbia, MO (Kremer 1987, 1993; Kremer et al. 
1990). Bacteria also were found to enhance symptom development caused by Colletotrichum 
truncatum on hemp sesbania (Schisler et al. 1991a), suggesting that an understanding of phyllosphere 
ecology may be valuable in optimal use of mycoherbicidal agents. 


Finally, experiments with a registered biological control agent transformed with a gene for herbicide 
resistance are being conducted at Beltsville, MD, and in containment at Frederick, MD (Brooker et 
al. 1993). 


ARS and other plant pathologists engaged in research on biological control of weeds with plant 
pathogens have been regular attendees at conferences and workshops on biological control and 
related issues (Battenfield 1983; USDA 1984a; Delfosse 1986, 1990; King et al. 1988; Coulson et al. 
1991; Lumsden and Vaughan 1993; Delfosse and Scott 1995), and several important international 
annual workshops organized under the Southern Regional Research Projects S-136 and S-234 
(Charudattan and Walker 1982). 


Significant accomplishments. During this period, the first foreign pathogens were purposely 
introduced and established in the field in the United States for biological control of weeds. Of the 
two pathogens introduced, one (Puccinia chondrillina) had previously been studied and introduced in 
Australia, and approval was obtained for its introduction into the United States after limited 
additional study. The rust is providing significant control of its targeted weed, rush skeletonweed, in 
western U.S. Research on the second exotic pathogen, Puccinia carduorum for musk thistle control, 
was conducted from start to finish by USDA-ARS. The research was conducted during a period when 
procedures for introducing biological control agents in the U.S. were undergoing increasing scrutiny 


90 


and change, which caused undue delay in obtaining approval for its release. Approval for 
experimental release of P. carduorum was recommended by the Working Group on Biological 
Control of Weeds in 1986, but final approval by the USDA for general use of the pathogen has not 
yet been received, after a period of over seven years. Once such final approval has been obtained, if 
such is obtained, the regulatory procedures developed during the approval process, and the research 
conducted to meet resulting regulatory requirements, will provide important precedents to guide 
future development of foreign pathogens for weed control. A third pathogen, a strain of Puccinia 
jaceae for yellowstar thistle control, is available for testing these new regulatory procedures. The 
Technical Advisory Group on Biological Control of Weeds gave a positive recommendation for field 
tests of this rust in 1990. Additional tests are to be conducted before final application for a release 
permit is made. . 


Much progress also has been made by ARS scientists for use of endemic pathogens for weed control. 
This is best exemplified by references cited above, and the following U.S. patents issued: Patent No. 
3,849,104 - Control of northern jointvetch with Colletotrichum gloeosporides f. sp. aeschynomene 
(Daniel at al. 1974); Patent No. 4,390,360 (Int. CI AO1N 63/04) - Control of sicklepod, showy 
crotalaria, and coffee senna with a fungal pathogen (Walker 1983); Patent No. 4,178,935 - Method 
for the preparation of mycoherbicide- containing pellets (Walker et al. 1988); Patent No. 4,902,333 - 
Patent on the concept of the invert emulsion (Quimby 1990); Patent No. 5,034,328 - Control of hemp 
sesbania with a fungal pathogen (Boyette 1991b); Patent No. 5,074,902 - Granular products 
containing fungi encapsulated in a wheat gluten matrix for biological control of weeds (Connick and 
Boyette 1991); and Patent No. 5,163,991 - Biocontrol of jointed goatgrass (Kennedy et al. 1992). 


D. BIOLOGICAL CONTROL OF PLANT NEMATODES. By R. M. Sayre 


In 1973, as a result of the agency wide reorganization of ARS mentioned in sections A and B.2, the 
Nematology Investigations unit ceased to be national in scope and its personnel of 28 scientists then 
located nationwide were reassigned to their respective regional and area management units. The 
single largest group of six scientists formed the Nematology Laboratory within the Plant Protection 
Institute (now Plant Sciences Institute) in the Beltsville Agricultural Research Center in Maryland. 
Leaders of this Laboratory have been R. Rebois (1974-85), R. N. Huettel (1985-1992), and D. J. 
Chitwood (1992-present). 


Early in this period, several nematicides were deregistered by action of the Environmental Protection 
Agency (EPA) and not allowed to be used on any crops. Consequently, nematologists were left with 
only five broad-use nematicides, four preplant fumigants, and six limited-use materials for making 
pest control recommendations (Feldmesser et al. 1985). Some nematode pest problems were not 
amenable to control by the remaining few materials as they were either ineffective or too costly for 
use on low value crops. As a consequence, control measures for nematodes were inadequate. 


Fortuitously, during this period B. R. Kerry of the Rothamsted Experiment Station in England, 
demonstrated that naturally-occurring fungi (i.e., four different fungal species) controlled the cereal 
cyst nematode (Kerry 1975, 1981). This was the first instance where soil microorganisms were found 
to be naturally suppressive to a population of pest nematodes. His discovery gave new impetus to 
research on soil fungi that attack eggs and other life stages of nematodes as possible biological 
control agents. Also this same year, a spore-forming bacterial pathogen was found to be an effective 
control agent for root-knot nematodes (Mankau 1975). These two discoveries set in motion renewed 
interest in using natural enemies of pest nematodes as control agents. 


R. M. Sayre of the Beltsville Nematology Laboratory has continued studies on the bacteria that 


parasitize nematodes, and in collaboration with M. P. Starr (University of California, Davis) in a 
series of studies on the spore-forming bacterial pathogens of nematodes, established the generic 


91 


designation Pasteuria for five bacterial species (Sayre 1980 a and b, 1988, 1993; Sayre and Starr 
1988, 1989; Sayre et al. 1991 a and b). These studies offered the means to others for identification of 
new isolates of the bacteria. In collaboration with N. A. Minton (ARS, Tifton, GA), it was 
determined through bioassays that endospores of Pasteuria penetrans were primarily responsible for 
a natural decline of the peanut root-knot nematode observed in field soils (Minton and Sayre 1989). 
While field observations indicated the potential of the bacterial group as control agents of pest 
nematodes, the inability to cultivate Pasteuria in vitro has prevented its commercial utilization. 


S. F. Meyer and colleagues of the Nematology Laboratory have isolated fungal parasites of the 
soybean cyst nematode (Meyer 1992; Meyer and Huettel 1993; Meyer et al. 1990). In particular, an 
isolate of Verticillium lecanii showing enhanced virulence to the nematodes has become the test 
organism in a technology transfer project with Crop Genetics International of Columbia, MD 
(Huettel and Meyer 1992). In August, 1992, Meyer and R. N. Huettel spent two weeks in China 
collecting fungal isolates found colonizing the life stages of soybean cyst nematode. These fungi 
were test organisms in a joint Sino-American Biological Control Laboratory project to find and 
utilize fungi as control agents for this pest nematode. 


In 1985, the Nematology Laboratory was divided, its taxonomists being transferred to a systematics 
laboratory (see also section B.2), leaving only three full-time nematologists in the Laboratory. The 
mission of the reduced laboratory was the development of new technologies to better manage 
plant-parasitic nematode pests by the use of safe, environmentally acceptable, control measures. This 
research effort included biological and bioregulatory control strategies as well as biochemical and 
molecular genetics, population dynamics, simulation modeling, and ultrastructure studies that 
provide a basic understanding of nematode biology. In 1989, the nematode taxonomists were 
returned to the Nematology Laboratory and the Laboratory mission once again included research on 
nematode taxonomy and insect-parasitic nematodes. 


Three ARS workshops have been held during this period to provide a forum to discuss relevant 
topics and a means of input into the planning process for future efforts in the area of biological 
control of soil pests. As a result, the Nematology Laboratory has a major commitment and defined 
mission in biological control of plant-parasitic nematodes. 


E. BIOLOGICAL CONTROL OF PLANT PATHOGENS. By R. J Cook, G. C. Papavizas, H. W. 
Spurr, C. L. Wilson, R. D. Lumsden, and C. R. Howell 


ARS research on biological control of plant pathogens during this last period has been conducted 
primarily at five locations: Work continued at the Beltsville, MD, and Pullman, WA, locations, and 
biological control studies on foliar pathogens and soilborne pathogens were begun at Oxford, NC, 
and College Station, TX, respectively, and three other locations, and on postharvest pathogens at 
Kearneysville, WV. Progress at each of these locations is discussed separately below. 


Beltsville, Maryland. At the time of the ARS reorganization in 1972, the Microbiology Group was 
separated from the Mushroom Group, and was renamed Soilborne Diseases Laboratory (SBDL), 
which was placed in the newly created Plant Protection Institute at the Beltsville Agricultural 
Research Center. G. C. Papavizas was named Chief of the new research unit, serving as leader of the 
unit from 1972-92. 


The next 21-year period could easily be divided into two periods, 1973-78 and 1979-93. The first of 
the two periods was characterized by the reintroduction of the "Mass Introduction and 
Augmentation" concept in plant pathology. As noted in sections above, the concepts of deliberate 
mass introduction and augmentation of beneficial organisms to control plant diseases was not very 
popular among plant pathologists, including those in USDA, because of early failures and because of 


92 


S. D. Garrett's first book (Garrett 1956). According to Garrett, a British plant pathologist, the attempt 
to increase the population of beneficial organisms in the soil was believed contrary to the ecological 
principle that the population reflects the habitat and that introduced changes are only transient. 
Although this concept is largely true, notable exceptions began to appear in plant pathology in the 
early 1970s. H. D. Wells, ARS plant pathologist at Tifton, GA, working with two Georgia scientists, 
was among the first to report use of Trichoderma preparations for field control of Sclerotium blight 
on peanuts (Wells et al. 1972). Their system was based on the introduction of the beneficial fungus to 
soil together with large amounts of organic matter to sustain augmentation of the antagonist. 


During the 1973-78 period, scientists of the SBDL at Beltsville obtained biological control of black 
root rot of bean (Thielaviopsis) by adding to soil industrial by-products (soybean cake, castor 
pomace, cotton seed cake) high in unsaturated fatty acids. They also isolated unsaturated fatty acids 
from the plant rhizosphere. These acids stimulate spore germination of the pathogen followed by 
lysis and destruction of propagules before infection can take place (Papavizas and Kovacs 1973). 
Concurrently, the SBDL developed a control system for Aphanomyces root rot of peas with 
cruciferous amendments added to soil and unravelled the mechanism of action which involved the 
decomposing action of soil microbes (Lewis and Papavizas 1973). 


An IPM breakthrough in the control of fruit rot of cucumber and root rot of bean caused by 
Rhizoctonia was also achieved in the SBDL at the same time. The IPM approach involved normal 
plowing (8-9. inches deep) instead of disking, use of the biological control agents Trichoderma and 
Corticium, and very small amounts of registered fungicides (Lewis and Papavizas 1980). 


Impressive advancements in the biological control of plant diseases in the Beltsville unit occurred 
from 1979-93. The unit's name was changed from Soilborne Diseases Laboratory to Biocontrol of 
Plant Diseases Laboratory (BPDL) in 1987, and was placed in the Plant Sciences Institute (PSI), 
created in 1985. Upon retirement of Papavizas in 1992, R. D. Lumsden was appointed Research 
Leader of the BPDL. At the establishment of the BPDL in 1987, most importantly, all scientific and 
material resources of the laboratory were redirected towards one goal only, viz., biological control of 
plant diseases with emphasis on soilborne diseases. 


During this last 15 year period, unit scientists discovered two unusual beneficial fungi, Sporidesmium 
sclerotivorum and Teratosperma oligocladum, on sclerotia of the soilborne plant pathogen 
Sclerotinia in soil at Beltsville. Sporidesmium parasitizes and destroys the survival structures 
(sclerotia) of Sclerotinia and can control this pathogen in the field for three consecutive years with a 
single application to soil (Adams and Ayers 1981; Ayers and Adams 1979, 1981; Uecker et al. 1978, 
1980). The BPDL received a U.S. Patent (No. 4,246,258, 1982) on Sporidesmium and is now in the 
process of transferring the biological control technology to industry. At the same time, other BPDL 
scientists developed for the first time in plant pathology new genetic variants of the biological 
control agents Trichoderma harzianum, T. viride, Gliocladium virens, and Talaromyces flavus (U.S. 
Patent No. 4,489,161, 1984) that possess enhanced abilities to control plant diseases and resistance to 
MBC fungicides, a major group of commonly used pesticides (Papavizas et al. 1982; Papavizas and 
Lewis 1983). Also, the BPDL developed liquid fermentation technology and an innovative 
encapsulation system for slow release of biological control agents and for field delivery (U.S. Patent 
Nos. 4,668,512, 1987, and 4,724,147, 1988) (Fravel et al. 1985; Lewis and Papavzas 1987b; Lewis et 
al. 1985; Papavizas et al. 1984). 


It was during this period that BPDL scientists established the importance of the chlamydospore of 
Trichoderma and Gliocladium in survival of these biocontrol agents in soil and in the eventual 
formulation of the biomass produced during liquid fermentation (Lewis and Papavizas 1984a; 
Papavizas et al. 1984). In 1984, the effectiveness of applying bran preparations containing young, 
actively-growing hyphae (3-day-old) of Trichoderma species and G. virens to reduce the pathogens 


o3 


Rhizoctonia, Pythium, and Sclerotium was reported (Lewis and Papavizas 1984b, 1987a). For the 
first time, it was shown that these young hyphae (germlings) of the biocontrol fungi significantly 
reduced pathogen inoculum with a decrease in disease, whereas conidial preparations were 
ineffective. 


In addition to these outstanding discoveries, BPDL scientists described potential commercial 
biological control systems for Sclerotium blight of bean (Papavizas and Lewis 1989b), Verticillium 
wilt of potato and eggplant (Marois et al. 1982), Rhizoctonia scurf of potato (Beagle-Ristaino and 
Papavizas 1985), Fusarium wilt of chrysanthemum (Locke et al. 1985), and Rhizoctonia and Pythium 
damping-off of ornamental plants (Lumsden and Locke 1989). In biocontrol studies of more basic 
nature, the mechanisms were elucidated by which the antagonists Talaromyces attacks Verticillium 
(Kim et al. 1988), Sporidesmium attacks Sclerotinia (Adams et al. 1985), Trichoderma and 
Gliocladium attack Rhizoctonia (Lewis and Papavizas 1987c; Lewis et al. 1991), and Gliocladium 
attacks Pythium ultimum (Lumsden et al. 1992; Roberts and Lumsden 1990). Also, research has been 
initiated to determine the genetic basis for biocontrol and for antagonist resistance to pesticides 
(Ossanna and Mischke 1990) as well as on the application of rhizosphere bacteria for biocontrol 
(Roberts et al. 1992). Considerable effort has also been given to the development of potential 
biocontrol fungi in the genera Laetisaria, Stilbella, and Cladorrhinum which have not previously 
been studied to any great extent (Lewis and Papavizas 1988, 1992, 1993). 


In the culmination of several years of research effort on the part of BPDL scientists in cooperation 
with W. R. Grace Company, the first fungal biocontrol formulation developed in the United States 
against plant pathogens received registration by the Environmental Protection Agency (EPA) in 1991 
(Lumsden et al. 1991). The formulation is an alginate prill (pellet) containing a food base (wheat 
bran) and biomass of G. virens (Gl-21) which is registered for use against Pythium and Rhizoctonia 
damping-off of vegetables and ornamental seedlings grown in commercial greenhouses (Lumsden 
and Locke 1989). The prill is produced by an industrial process and, in 1992, was test-marketed in 
several states. The use of the prill formulation on high-value field crops may eventually be feasible, 
since beneficial effects of the Gl-21 prill (GlioGard™) on diseases of tomato and pepper in the field 
caused by Sclerotium rolfsii were observed (Ristaino et al. 1991). A novel formulation consisting of 
vermiculite/bran and activated biomass of various isolates of Trichoderma spp. and G. virens has 
been patented recently by the BPDL (U.S. Patent No. 5,068,105, 1991) and shows potential against 
diseases caused by Rhizoctonia solani (Lewis et al. 1991). 


Results of these and other biological control research activities of the Beltsville Laboratory also 
appear in various reviews and book chapters, some of which are: Adams and Ayers 1981; Fravel 
1988; Harman and Lumsden 1990; Lewis 1991; Lumsden 1992; Lumsden and Lewis 1989; Lumsden 
and Papavizas 1988; Papavizas 1984, 1985, 1987; Papavizas and Lewis 1981, 1989a; Papavizas and 
Loper 1986; Papavizas and Lumsden 1980; and in the proceedings of Beltsville Symposium XVIII 
(Lumsden and Vaughn 1993). 


Pullman, WA. A landmark event in biological control of plant pathogens occurred in 1974, with the 
publication of the first book wholly devoted to the subject. This book was coauthored by K. F. Baker, 
a retired University of California professor and ARS collaborator, and R. J. Cook, an ARS plant 
pathologist at the ARS Regional Cereal Disease Research Laboratory at Washington State 
University, Pullman (Baker and Cook 1974). A second book on the subject by the same two authors 
was published nine years later (Cook and Baker 1983). 


Using the two-step approach outlined in the 1974 book, i.e., 1) to find effective antagonists, look 
where the disease does not occur but should, and 2) then isolate candidates from plant parts where 
protection is needed, scientists from the Pullman unit, working cooperatively with scientists from 
England and Australia, obtained evidence that the biological factor responsible for take-all decline in 


94 





wheat was transferable from soil to soil, and was active in the rhizosphere or possibly within the 
roots of the protected wheat. They isolated several flourescent Pseudomonas strains from the 
protected roots and showed the potential of these bacteria to duplicate the suppressive effect typical 
of soil from fields where take-all had declined (Cook and Rovira 1976). The Pullman scientists then 
showed that the soils change microbiologically, both quantitatively and qualitatively, toward higher 
populations of fluorescent Pseudomonas species inhibitory to the take-all fungus as the soil converts 
from conducive to suppressive during take-all decline (Weller and Cook 1983). They obtained the 
first experimental evidence in the field that take-all of wheat could be suppressed by simply treating 
the wheat seeds with one or more strains of inhibitory pseudomonads (U.S. Patent No. 4,456,684). 
They then demonstrated that Pythium root rot of wheat could also be suppressed to a significant 
degree by treatment of wheat seeds at planting with one or more strains selected for ability to inhibit 
this pathogen (U.S. Patent No. 4,647,533). 


In 1987, Pullman scientists presented proof based on both genetic evidence and direct isolation from 
rhizosphere soil that the protection afforded wheat roots by at least two fluorescent Pseudomonas 
species resulted from ability of these species to produce phenazine-type antibiotics (Thomashow and 
Weller 1988). Soil microbiologists and plant pathologists had debated since the 1940s and earlier 
whether antibiotics played any role in the ecology of soil microorganisms or in biological control of 
root pathogens by antagonists. Pullman scientists used Tn5 mutagenesis to produce mutant strains 
identical to the parental (wild-type) strain but unable to produce phenazine because of the 
inactivization of a single gene (Thomashow and Weller 1988). These strains retained some residual 
biological control activity against take-all when introduced into the rhizosphere of wheat by seed 
inoculation (indicating more than one mechanism of inhibition), but they were markedly less active 
than their parents. Restoration of antibiotic production by complementing the inactivated DNA 
sequence with DNA introduced from a library of parental DNA coordinately and fully restored 
biological control activity. The Pullman workers then demonstrated by use of analytic chemical 
techniques that both the parent and complemented strains, but not the mutant strain, produced 
phenazine in the rhizosphere of wheat growing in natural soil (Thomashow et al. 1988). 


The ARS group at Pullman in cooperation with scientists at the Monsanto Company, St. Louis, MO, 
have subsequently demonstrated a role of the antibiotic phloroglucinol in the biological control of 
wheat take-all by other strains of fluorescent pseudomonads (Vincent et al. 1991). Again, the tools of 
recombinant DNA (rDNA) technology were used to produce antibiotic-negative mutants, restore 
antibiotic producing ability, and prove the role of antibiotic production in biological control. 


The demonstrations by the ARS unit at Pullman that wheat root diseases can be controlled by 
microorganisms introduced into the rhizosphere parallels several similar studies by workers in other 
federal (see College Station, TX, paragraphs below) and state experiment station laboratories, private 
companies, and in other countries on biological control of plant pathogens with plant-associated 
microorganisms. The first and still most successful example of this approach to biological control is 
work in Australia just previous to this period on control of crown gall caused by Agrobacterium 
tumefaciens, by prior establishment on the plant of populations of avirulent strains of Agrobacterium 
radiobacter K84 (New and Kerr 1972). These types of studies, and the new tools of rDNA 
technology, have ushered in approaches to "biological control" very different from the original 
approaches of C. V. Riley and other early entomologists. This in turn has reopened discussions of 
previous years over the definition of the term "biological control" (see Introduction to this history). 


College Station, TX. Research on the biological control of cotton seedling diseases was initiated at 
the Cotton Pathology Research Unit (CPRU) of the Southern Plains Area in 1978 when C. R. Howell 
was relieved of work on Verticillium wilt and given responsibility for seedling disease research. By 
1979, work was completed on the use of a strain (Pf-5) of Pseudomonas fluorescens to control cotton 
damping-off incited by Rhizoctonia solani (Howell and Stipanovic 1979). Control was ascribed to 


25 


production of the antibiotic pyrrolnitrin that was isolated and characterized from the bacterium. In 
1980, strain Pf-5 of P. fluorescens was shown to suppress cotton seedling damping-off incited by 
Pythium ultimum, and control was ascribed to production of the antibiotic pyoluteorin by the 
bacterium (Howell and Stipanovic 1980). Also, in 1980-82, the use of the mycoparasitic fungus 
Gliocladium virens to control damping-off of cotton seedlings incited both by R. solani and P. 
ultimum was described (Howell 1980, 1982). 


In 1983, an antibiotic strongly inhibitory to P. ultimum was isolated and described from a strain of G. 
virens (Howell and Stipanovic 1983). This newly discovered compound was named "glioviren," and 
its production was demonstrated to be a major factor in suppression of Pythium damping-off by G. 
virens. In 1984, a potent phytotoxin was isolated from cultures of G. virens and shown to cause 
necrosis of emerging seedling radicals (Howell and Stipanovic 1984). This compound was identified 
as viridiol, a reduced form of the antibiotic viridin, and preparations of G. virens containing this 
material were shown to be effective in controlling weed infestations in cotton field soil. (All 
identification and characterization of compounds isolated from bacteria and fungi were done in 
collaboration with R. D. Stipanovic, ARS, College Station.) In 1987, it was demonstrated, through 
the production of parasitic deficient mutants, that mycoparasitism was not an important mechanism 
in the control of R. solani-incited seedling disease by G. virens, and disease control was ascribed to 
antibiotic production by the antagonist (Howell 1987). 


From 1988-90, collaborative research with Ciba-Geigy Corporation resulted in patent applications 
for use of six bacterial strains for control of seedling damping-off, the use of bacterial and fungicide 
combinations for seedling disease control, and for genes coding for or promoting antibiotic synthesis 
in bacteria. Also, the primary mechanism in the biocontrol of Pythium damping- off of cotton 
seedlings by Enterobacter cloacae was found to be the production of ammonia from seed exudates 
by the bacterium (Howell et al. 1988). In 1991, strains of G. virens were separated into two distinct 
groups on the basis of their antibiotic production in vitro; Q strains were found to produce gliotoxin, 
while P strains produced only gliovirin (Howell and Stipanovic 1991). Also, a seed treatment method 
was developed to control Pythium damping-off of cotton seedlings with G. virens (Howell 1991); 
biocontrol efficacy depended on the strain of the fungus and the substrate on which it was grown. A 
method was developed to suppress phytotoxin (viridiol) production in cultures of G. virens by the 
addition of low concentrations of sterol-inhibiting fungicides to the growth medium and to the air 
dried preparations to prevent subsequent production (Howell and Stipanovic 1993); this does not 
suppress the fungal growth rate or production of antibiotics. 


Oxford, NC, and other locations. Research on the biological control of foliar plant pathogens has 
been conducted at four locations during this period. Research at the ARS Crops Research Laboratory 
(prior to 1987 the Tobacco Research Laboratory) at Oxford, NC, under the leadership of H. W. 
Spurr, was conducted 1970-present. One of the primary objectives of this research has been to 
develop practical biological control methods or strategies for foliar diseases of tobacco and peanut. 
Research began in 1970 with the characterization of epi- and endophytic fungi in tobacco leaves in 
relation to the development of Alternaria leaf spot disease (Spurr and Welty 1975). 


Inoculations of leaves with spores of nonpathogenic Alternaria alternata isolates decreased 
infections by pathogenic fungi (Spurr 1977). Various possible mechanisms for this biological control 
activity were considered, including toxin production, phytoalexin induction in the plant, and nutrient 
competition on or within the plant (Blakeman and Fokkema 1982). The mycelial growth of 
nonpathogenic A. alternata on the leaf surface was often colonized by bacteria which caused lysis. It 
was considered that these bacteria, in conjunction with the nonpathogenic A. alternata, controlled 
pathogenic A. alternata. Two investigations were then initiated. 


96 


In one test, a 70% ethanol treatment of leaf tissue was devised which decreased normal, resident, 
bacterial and fungal leaf microflora of greenhouse-grown tobacco leaf tissue by 91 and 100%, 
respectively (Spurr 1979). Protective biological control of Alternaria leaf spot resulting from 
application of nonpathogenic A. alternata spores was effective on both ethanol-treated and untreated 
leaf tissue, indicating nonpathogenic spores controlled leaf spot without interacting with other leaf 
surface microorganisms; but this does not mean that such interactions do not occur, thereby altering 
control efficacy. 


In the second study, tobacco leaf surface bacteria were isolated and bioassayed for control of A. 
alternata (Fravel and Spurr 1977). One active isolate, identified as Bacillus mycoides (as cereus var. 
mycoides), prevented leaf spot disease in a controlled environment. After this discovery, bacterial 
strains, such as Bacillus thuringiensis (Bt), sold in commercial formulations to control insects, were 
tested. The Bt strain HD-1 was found to be equivalent to B. mycoides. A gram negative bacterium 
isolated from a pathogenic corn fungus in Ohio (Sleesman and Leben 1976), identified as 
Pseudomonas cepacia (Pc 742), was also active. The gram negative Pc 742 and the gram positive 
HD-1 strains were field tested for control of Alternaria leaf spot and peanut Cercospora leaf spot 
caused by Cercospora arachidicola. The tests in peanuts demontrated that this biological control 
approach was inconsistent, control varying from 20 to 70%, being more efficacious than some 
fungicides, but poorer than recommended fungicides (Knudsen and Spurr 1987). Bacterial numbers 
decreased dramatically following application to foliage. 


Survival of antagonists introduced into the phylloplane is required to effect control, and equals the 
importance of the antagonistic potential of the biological control organism. It is suggested that the 
most effective method of foliar biological control is to begin with a bacterial epiphyte, one 
well-suited to the leaf surface environment and known to multiply (Leben 1974; Knudsen and Spurr 
1988). Research on the phylloplane (Spurr 1990) is continuing at Oxford, which is the only ARS 
location where such research has been done (until recently; see below). 


An important event for biological control of foliar pathogens occurred in 1984 with the Symposium 
entitled "Biological Control Strategies in the Phylloplane" held in conjunction with the annual 
meeting of the American Phytopathological Society in August of that year at Guelph, Ontario. 
Participants of this Symposium included ARS scientists from the Oxford laboratory and a number of 
scientists from several state agricultural experiment stations and U.S. and Canadian universities; the 
proceedings of the symposium were published in 1985 (Windels and Lindow 1985). 


A second plant pathologist, V. J. Elliott, was recruited in 1990 at Oxford, the first plant pathologist 
employed by ARS to research biological control of foliar pathogens full time. The main thrust of 
research currently (1993) in progress is to develop an extensive description of epiphytic and 
endophytic microorganisms of foliage with emphasis on peanut and tobacco. The response of 
phyllosphere microfloral populations to environment and other dynamics must be understood prior to 
introducing microbes for control of foliar diseases. 


There are several ARS projects on biological control of foliar pathogens that have been part of other 
research programs or are of recent origin. Research at Beltsville, MD, was conducted at the Fruit 
Laboratory by E. L. Civerolo from 1984 until 1988, when he became National Program Staff Leader 
responsible for plant pathology. He studied and characterized bacterial strains of Xanthomonas 
campestris pvs. pruni and citri, pathogens of fruit and foliage of peach and citrus trees, respectively. 
Bacteriophages, viruses which lyse bacterial cells, were isolated, identified and tested as biological 
control agents for these bacterial pathogens. The results demonstrate the feasibility of biological 
control using pruniphage as an alternative disease management strategy to chemical sprays 
(Randhawa and Civerolo 1986). Research at the Microbiology and Plant Pathology Laboratory at 
Beltsville resulted in the discovery and patenting of a strain of Bacillus subtilis, which when sprayed 


27 


on bean leaves controls rust (Baker and Stavely 1986). Various formulations were tested in field 
studies. Effective control was obtained only if the bacterial formulation was applied every other day. 
Studies of the mechanisms were also made but were unsuccessful. These discouraging events have 
led to a discontinuation of this research. 


Cooperative research at the ARS U.S. Regional Pasture Research Laboratory at University Park, PA, 
and Pennsylvania State University, has resulted in the isolation of bacterial strains from ecosytems 
for testing as biological control agents for forage legume diseases. Emphasis is on control of alfalfa 
leaf spot caused by the fungal pathogen Phoma medicaginis, on survival of bacteria following 
introduction to leaf surfaces, and on evaluation of the impact of various formulation ingredients and 
combinations of bacterial strains (Jones et al. 1987). 


Various wheat lines, resistant and susceptible to Septoria leaf blotch and Pyrenophora tan spot, are 
being evaluated for their potential to host leaf colonizing bacteria antagonistic to these fungal 
pathogens at the ARS Plant Science and Water Conservation Research Laboratory at Stillwater, OK. 
Of the leaf colonizing bacteria isolated, one strain of Pseudomonas fluorescens was inhibitory in 
vitro to the growth of the above fungal pathogens. Two toxic products were isolated from this 
bacterial strain (Gough and El-Nashaar 1989). 


Kearneysville, WV. Research on the biological control of postharvest pathogens was conducted 
primarily at the ARS Appalachian Fruit Research Station (AFRS) at Kearneysville, WV, during this 


period. Chemical pesticides have been one of the major methods for controlling postharvest losses of 
food. Incidents in the 1980s involving food contamination with pesticides heightened public 
awareness of pesticide residues in food. In addition, a 1987 National Academy of Sciences report on 
food safety (NRC, 1987) indicated that fungicides used to preserve food posed more of an oncogenic 
risk than other pesticides. Also, resistance of microorganisms to fungicides applied after harvest has 
occurred rather frequently. Thus a critical need developed for alternatives to synthetic fungicides for 
the control of postharvest diseases of fruits and vegetables. The biological control research program 
of the AFRS has been directed toward addressing this need. The pathology group at the AFRS, under 
the initial leadership of C. L. Wilson, has since 1984, accelerated and expanded its research program 
on the biological control of postharvest diseases and fire blight. The program has involved the use of: 
1) antagonistic microorganisms; 2) natural fungicides; and 3) induced resistance as alternatives to 
synthetic fungicides. Some results of this research are summarized below. 


In a 1982-84 postdoctoral study by P. L. Pusey in association with the AFRS, an isolate of Bacillus 
subtilis was discovered that effectively controlled brown rot of peaches caused by Monilinia 
fructicola, A patent was issued covering this process and a license has been issued to ISK 
Technologies to develop a marketable product. (Pusey and Wilson 1984; Pusey et al. 1986, 1988). 
This was the first patent of a microorganism to control postharvest diseases of fruits or vegetables. 


In 1984, research was initiated on the biological control of pome fruit rots at Kearneysville by 

W. Janisiewicz. A number of antagonists were discovered that are effective against Botrytis cinerea, 
Penicillium expansum, and Mucor rots of apple and pear, and patents were issued on the use of the 
antagonists Acremonium breve and Pseudomonas cepacia against pome fruit rots (Janisiewicz 1987, 
1988 a and b; Janisiewicz and Roitman 1988). The firm EcoScience has licensed these patents and is 
attempting to commercialize this technology. 


In cooperative ARS-Israeli research under the Binational Agricultural Research and Development 
(BARD) program, a number of antagonistic yeasts active against postharvest rots of citrus and 
deciduous fruits have been discovered. Two of these, Candida guilliermondii (strain US-7) and C. 
oliophila, were found to have broad-spectrum activity against a number of rot fungi on a variety of 
fruit including citrus, pome fruit, grapes, persimmon, and tomatoes (Wilson and Chalutz 1989; 


98 


Wilson et al. 1993). Ecogen has licensed the patents on these organisms and is attempting to 
commercialize them. 


In 1987, research was initiated at the ARS Blueberry and Cranberry Research Center at Chatsworth, 
NJ, to find antagonists that would control postharvest rots of cranberries and blueberries. One 
antagonist has been found that is effective against Alternaria rot of blueberries. In 1988, studies were 
begun by T. van der Zwet at the AFRS to find antagonists for biological control of the fire blight 
organism, Erwinia amylovora. The probability that streptomycin presently used to control fire blight 
may be withdrawn from the market makes this research particularly timely. 


Other research at the AFRS includes studies by M. Wisniewski on the mode of action of various 
antagonists of fruit rot pathogens. Cooperative research has shown that an antagonist of Rhizopus rot 
of peaches, Enterobacter cloacae, and the broad-spectrum antagonist Candida guilliermondii (strain 
US-7) express their antagonism primarily through nutrient competition. It has also been shown that 
some yeast antagonists are able to attack rot pathogens directly and degrade their cell walls 
(Wisniewski et al. 1988, 1989, 1991 a and b; Droby et al. 1989). 


AFRS researchers are conducting cooperative research with other U.S. and foreign investigators. A 
large scale test was conducted in cooperation with the ARS Southeastern Fruit and Tree Nut 
Research Laboratory at Byron, GA, to evaluate Bacillus subtilis for brown rot control under 
commercial conditions. 


Cooperative research with Cornell University concerns cytological experiments on 
antagonist/host/pathogen interactions. Cooperators at the ARS Western Regional Research Center in 
Albany, CA, and the ARS Agricultural Research Center, Athens, GA, have helped characterize the 
antibiotics produced by two of the biological control agents found at the AFRS. Testing under 
storage conditions of some of the apple pathogen antagonists is underway at the ARS Tree Fruit 
Research Laboratory at Wenatchee, WA. The AFRS is also cooperating with the Volcani Institute in 
Israel and the Institute for Crop and Food Research, Levin, New Zealand. And research has been 
initiated at Kearneysville on the microecology of fruit surfaces as it relates to biological control, and 
on resistance in fruit that may be induced by antagonistic microorganisms and low-dose UV light. 


In addition to the references noted above, results of the research discussed above and other biological 
control studies of the pathology unit at the AFRS can be found in many of its publications; see 
Chalutz et al. 1988 a and b; Chalutz and Wilson 1990; Wilson 1977, 1989; Wilson and Chalutz 1989; 
Wilson and Pusey 1985; Wilson et al. 1987 a and b; Wisniewski et al. 1988, 1989; see also Sanchez 
1990. Several major reviews of the subject of biological control of postharvest diseases of fruits and 
vegetables have been authored by AFRS scientists (Janisiewicz 1988b, 1990; Wilson and Wisniewski 
1989, 1992, 1994; Wisniewski and Wilson 1991; Wilson et al. 1991). 


In September 1990, an international workshop sponsored by the BARD program was hosted by the 
AFRS on the "Biological Control of Postharvest Diseases of Fruits and Vegetables." This workshop 
brought together for the first time government and university reseachers with industry representatives 
who were interested in developing alternatives to synthetic fungicides for the control of postharvest 
diseases (Wilson and Chalutz 1991). A number of cooperative research projects and agreements 
resulted from this meeting. 


99 


CHAPTER V 
1953-1993 
FOREST SERVICE - OVERVIEW 
By Mary Ellen Dix 


The use of parasites, predators, and pathogens to control insect, disease-causing, and weed pests of 
trees is not a new idea in the United States. Natural enemies have been imported or manipulated to 
control tree pests for over 90 years. Prior to 1953, researchers of the U.S. Department of 
Agriculture's (USDA) Bureau of Entomology and Plant Quarantine (BEPQ) were responsible for 
biological control research and implementation on native and exotic forest pests. Their studies were 
designed to obtain information on the identities, distributions, and biologies of natural enemies of 
insects and pathogens of native trees, and of exotic pests in their home range whenever possible. 
Many parasites and predators were introduced and released for control of forest pests, especially 
pests of European origin (Clausen 1956, 1978; Schaffner 1959; Dowden 1962). 


In 1954, the USDA was reorganized and the responsibility for biological control of forest pests was 
transferred from the BEPQ to the Forest Service. Many entomologists and pathologists, including 

P. B. Dowden, B. H. Kennedy, C. L. Massey, J. A. Beal, F. G. Hawksworth, and N. D. Wygant 
transferred from the Bureau to the Forest Service where they continued their biological control 
research and implementation activities. However, many research papers, reports, and parasite 
releases during the late 1950s and early 1960s were the result of initial work by the Bureau (Clausen 
1956; Schaffner 1959; Dowden 1962; see Chapters I and II). 


This overview and Appendix III summarize biological control research and application efforts in the 
Forest Service from 1953 to present. The overview briefly describes the trends and directions of 
biological control; however, it is not all inclusive. Appendix III contains detailed information on 
biological control activities, arranged by pest, and includes literature references to the studies briefly 
reported in this overview. 


Organization of the Forest Service. In 1954, the Forest Service was divided into three branches: 
Research, State and Private Forestry, and the National Forest Administration. All insect and disease 
research and survey activities were administered by the Research branch. Forest Insect Research and 
Forest Disease Research staffs in the Washington Office (WO) were separate staffs with their own 
directors, but were administered by the Assistant Chief for Research. In about 1960, Forest Pest 
Control (survey) was split from Research and placed in State and Private Forestry, Forest Insect and 
Disease Management (FIDM). The Insect and Disease Research staffs were later combined into 
Forest Insect and Disease Research (FIDR). The Director of FIDR reported to the Associate Deputy 
Chief for Research who in turn reported to the Deputy Chief for Research. During the 1960s, the 
number of Forest Experiment Stations decreased from nine to eight in addition to a Forest Products 
Laboratory. During this same period the number of Regions decreased from ten to nine. Each 
Experiment Station contained numerous research laboratories, and each Region had several field 
offices (Steen 1976). 


100 


State and Private Forestry (Forest Health) was and remains responsible for providing leadership and 
assistance for the protection, management, and effective use of 574 million acres of non-federal 
forests and grasslands (Rietveld 1993). In 1975, Forest Insect and Disease Research (FIDR) became a 
separate organization under the Associate Deputy Chief in the Office of the Deputy Chief for State 
and Private Forestry (Steen 1976). The name was shortened to Forest Pest Management (FPM) 
during the 1980s and changed to Forest Health in 1993. 


The Forest Service is currently divided into six Branches: Research, State and Private Forestry, 
National Forests, International Forestry, Administration, and Programs and Legislation. 
Responsibility for biological control of forest pests falls within the missions of both the Research and 
State and Private Forestry (Forest Health) Branches. International Forestry facilitates and helps 
coordinate foreign activities of these two branches. 


Before 1980, the WO staffs strongly influenced the direction of biological control research and 
implementation activities in all Experiment Stations and Regions. After 1980, the WO staffs served 
in an advisory role, while the Station Directors and Regional Foresters were responsible for 
formulating program directions. 


Biological Control Activities, 1954-1969. The overall mission of FIDR from 1954 to 1970 was the 
"development of safer and more economical methods of direct and preventive control of forest pests" 
(USDA Forest Service 1962). This mission included completion and publication of results of studies 
and surveys initiated under the BEPQ. Such studies centered on identifying forest pests, determining 
their distribution and documenting aspects of their biologies and that of their natural enemies. For 
example, J. V. Schaffner, Jr., published information on the identity, distribution, and biology of 
parasites reared from microlepidoptera in the northeastern United States between 1915 and 1959 
(Schaffner 1959; Clausen 1978). The passage of the Forestry Research, State Plans, and Assistance 
Act (McIntire-Stennis) in 1962 facilitated these kinds of efforts by authorizing federal support for 
forestry research on the biological control of forest pests at land grant universities. 


Public Law 480 (PL-480) projects also were used to help identify exotic parasites of introduced 
forest pests in their native land. In 1960, ten PL-480 projects were funded in five countries. By 1965, 
there were 27 projects in nine countries (Finland, Poland, Spain, Pakistan, India, Yugoslavia, Brazil, 
Colombia, and Uruguay). Through these projects, parasites, predators, and pathogens were identified 
for gypsy moth, European pine shoot moth, "tip moths" (Rhyacionia spp.), balsam woolly adelgid, 
smaller European elm bark beetle, and various sawflies. (Scientific names and orders and families of 
organisms mentioned in this Chapter are listed in the Index.) In addition, Agricultural Research 
Service (ARS) scientists at overseas laboratories collected natural enemies that were subsequently 
identified at their Systematic Entomology Laboratory, headquartered at Beltsville, Maryland. 
Candidate natural enemies were shipped to the ARS quarantine facilities in Moorestown, NJ 
(Newark, DE, after 1973), for initial clearance and biological evaluations before being sent to the 
appropriate Forest Service facility for further biological evaluations and impact studies. 


Most of the insect pests and pathogens targeted for biological control within the different Experiment 
Stations and Regions caused localized problems; however, a few were of regional, national or 
international importance (Table 3). In the Pacific Northwest, including Alaska, parasites were 
released for control of the Douglas-fir beetle and larch casebearer. Concurrently, natural enemies 
were identified for the western blackheaded budworm, western spruce budworm, hemlock looper, 
Douglas-fir tussock moth, and the pine tip moths (Rhyacionia spp.). In California and the Pacific 
Islands, scientists identified hymenopterous and nematode parasites, and avian predators of seed and 
cone insects and beetle borers. Scientists also evaluated the impact of Bacillus thuringiensis (Bt) on 
populations of the "Great Basin tent caterpillar". Parasites, birds, nematodes and other natural 
enemies of spruce budworms, spruce beetle, Engelmann spruce weevil, and Douglas-fir beetle were 


101 


identified by scientists in the Intermountain and Pacific Northwest Regions. Scientists working 
within the Stations and Regions now within the Rocky Mountain Station identified nematodes, mites, 
and arthropod parasites and predators of the western spruce budworm, spruce beetle, and various 
pine bark beetles. 


In the eastern United States, natural enemies were released for control of the smaller European elm 
bark beetle, balsam woolly adelgid, larch sawfly, red pine scale, European pine shoot moth, 
European pine sawfly and elm spanworm. Bt strains were evaluated for control of the "eastern" 
spruce budworm and gypsy moth, as were other pathogens. Predators and parasites were identified 
for cankerworms, gypsy moth, "forest budworms", southern pine beetle and other bark beetles. 
Southern biological control efforts were primarily concerned with identifying natural controls of the 
black turpentine beetle, southern pine beetle, hardwood borers, and Cydia (=Laspeyresia) spp. See 
Appendix III for details of these programs, and of those noted below. 


Biological Control Activities, 1970-1979. Biological control efforts in the 1970s were shaped by 
several events. During the early 1970s, severe outbreaks of the gypsy moth, southern pine beetle, and 


Douglas-fir tussock moth resulted in a public and congressional call for their suppression. In 1972, 
EPA banned the use of DDT, a commonly used and potent insecticide, because it was hazardous to 
the environment. The publication of "Silent Spring" (Carson 1962) and other environmental 
publications, increased public concern about the environment and its pollution, particularly by 
chemical pesticides. Conversely, the adverse impacts of imported pests, and potential adverse 
impacts of imported natural enemies, also became of concern. During the 1970s, the Forest Service 
approached pest control in a more systematic manner than previously in the 1950s and 1960s. 
However, only a few serious pests were targeted. The concept of integrated pest management (IPM) 
gained popularity in forestry. A variety of methods and a highly flexible planning base were used to 
cope with pests on a long-term basis. IPM enabled forest resource managers and pest control 
specialists to manage trees for specific objectives (Miller et al. 1975). 


Also, during the 1970s, biological control research was slowly deemphasized as research efforts 
increased on pheromones, impacts, biologies, and chemical controls of major insect pests and 
pathogens (Table 3). Identification of natural enemies of many forest insects continued, but usually 
as a secondary endeavor. Most biological control research was targeted toward understanding the 
impacts of natural enemies on pest population dynamics, modelling natural enemy-pest interactions, 
or developing techniques for suppressing pest populations with microbials. Nuclear polyhedrosis 
viruses (NPVs) were successfully used against several sawflies and the Douglas-fir tussock moth, 
whereas Bt preparations gave encouraging results in experimental studies against gypsy moth, spruce 
budworms, forest tent caterpillar, and other defoliators (Abrahamson and Harper 1973). Natural 
enemies or potential enemies were identified for mountain pine beetle, dwarf mistletoes, Armillaria 
root rot, southern pine beetle, Douglas-fir tussock moth, Douglas-fir beetle, spruce budworm, gypsy 
moth, seed and cone insects, Fusarium spp., sawflies and a few minor pests. Control programs with 
parasites were implemented for the smaller European elm bark beetle and spruce budworm and with 
pathogens for southern pine beetle, gypsy moth, and Douglas-fir tussock moth. 


The 1970s are best known for the accelerated research and development programs ("big bug 
programs") to control severe outbreaks of the gypsy moth in the Northeast, the southern pine beetle 
in the South, and the Douglas-fir tussock moth in the Pacific Northwest. Between 1970 and 1973, 
outbreaks of these three pests severely damaged forests, causing huge losses in forest revenues. In the 
fall of 1973, the USDA Assistant Secretary of Agriculture for Conservation, Research and Education 
requested that the Forest Service (FS), Cooperative State Research Service (CSRS), Agricultural 
Research Service (ARS), and Animal and Plant Health Inspection Service (APHIS) all coordinate 
short-term programs to reduce damage caused by these three forest pests (Bayley 1981). In the fall of 
1974, Congress appropriated over $6 million above existing funds for major forest insect and disease 


102 


programs on these three pests. Research and development emphasis and objectives were slightly 
different for each accelerated regional program (Shea 1985). 


The Expanded Southern Pine Beetle Research and Application Program focused on understanding 
the population dynamics of the beetle; using beetle-killed trees, silvicultural techniques for 
prevention, and cut and leave techniques; developing integrated models for predicting impacts, 
population levels and forest susceptibility; and developing survey and suppression techniques with 
pheromones and insecticides. Research on potential biological control agents was not immediately 
addressed unless program management viewed the biological agents as critical to understanding the 
population dynamics of the pest, or to predict population trends (Thatcher 1981). Consequently, in- 
depth research on natural enemies was limited to a few species of predators and parasites. 


The Gypsy Moth Expanded Research and Application Program called for use of broad-based 
pesticides to control the moth; increased foreign exploration for parasites and predators; 
developmental research on microbial control; and increased research to analyze and predict changes 
in pest populations. In cooperation with ARS, a nuclear polyhedrosis virus (NPV) was produced in 
vivo. Eventually the virus was tested for environmental persistence, epidemiology, and efficacy, and 
later aerially applied to outbreaks. After completing safety evaluations per EPA regulations on safety 
testing of insect viruses, the gypsy moth NPV product (Gypchek™) was approved by EPA in 1978. 
During the 1970s, a few exotic parasites of gypsy moth were imported for evaluation and released by 
Forest Service scientists. None of these are at this time considered established. However, intensive 
field and laboratory trials collected data on the behavior, host selection, site preferences, and other 
information needed to evaluate impact and management of the parasites: Brachymeria intermedia, 
Cotesia (=Apanteles) melanoscelus, Blepharipa pratensis, and Compsilura concinnata. 
Augmentative release of these parasites in the Northeast also showed mixed results. Releases of other 
parasite species in combination with Br or NPV applications also had mixed results. In one study, 
where Bt was used in combination with C. melanoscelus, gypsy moth populations were lower and 
foliage protection was higher than when Bt was used alone. This parasite also has been implicated in 
the transmission of NPV (Doane and McManus 1981). Following the releases, research was 
accelerated on selection and evaluation of strains, formulations, and application techniques for Bt, 
NPV, and other pathogens. 


The Douglas-fir Tussock Moth Accelerated Research and Development Program focused on 
developing effective suppression techniques with NPV and Bz, obtaining information on natural 
enemies needed to predict population levels; and impacts of the pest. Intensive research by the insect 
pathology project personnel at Corvallis, OR, focused on virus strain identification, virus potency 
trials, and assessment of impacts on non-target organisms. Large-scale forest tests obtained data to 
optimize viral dosage, develop application strategies, and receive EPA approval for the registration 
of the NPV BioControl-1™ in 1976. Parasites and predators of Douglas-fir tussock moth were 
identified and their impacts on pest populations were assessed at high and low host population levels 
(Torgersen 1977, 1981; Mason and Overton 1983; Mason and Torgersen 1983; Mason et al 1983). 
Both the Douglas-fir tussock moth and gypsy moth programs were redirected into the spruce 
budworm program after the former terminated in the late 1970s. 


In 1977, the Canada/United States Spruce Budworms Program (CANUSA) was established similar to 
the Douglas-fir tussock moth and gypsy moth programs. This six-year research, development, and 
application program actively explored the identity and role of natural enemies in regulating pest 
populations. Methods were developed for suppressing "eastern" and western spruce budworm 
populations with natural enemies (Winget 1985). 


iological rol Activities, 1980- . Funding for Forest Service insect and disease research 
(FIDR) increased slightly during the 1980s. However, FIDR funding in terms of constant dollars 


103 


decreased by over 20% (Sesco 1992). FIDR was extensively reorganized and biological control 
research in the Forest Service came upon hard times. Research work units were merged and some 
programs were consolidated into centers while others were eliminated. As a consequence of such 
program reorganization, there were significant losses of qualified scientists working in biological 
control. F. B. Lewis and A. T. Drooz retired and other positions were lost. Many scientists were 
assigned to positions that did not include biological control. Such scientists had not only been 
instrumental in the development of biological control research within the Forest Service, but they 
also were pioneers in biological control of specific insects and diseases. Because of these changes, 
biological control research was reduced by the mid-1980s, and consequently limited to only a few 
locations and projects. Studies to identify and evaluate natural enemies diminished to secondary 
priority among other research areas. 


In 1980, a five-year Integrated Pest Management Program for Bark Beetles and Diseases of Southern 
Pines was initiated to complete research and transfer technical information from the Expanded 
Southern Pine Beetle Research and Application Program. This program also began developing an 
integrated southern pine pest management system for several species of bark beetles (southern pine 
beetle, black turpentine beetle, and Jps spp. "engraver beetles") and disease complexes (fusiform rust, 
annosus root rot, and littleleaf disease) of southern pines. Information on natural enemies was 
collected and summarized to improve the accuracy of population dynamics models (Shea 1985; 
Branham and Thatcher 1985). Findings and activities of these "big bug programs" are summarized by 
Sanders et al. (1985), Thatcher et al. (1981), and Doane and McManus (1981). These publications 
also listed research needs for improving methods of coping and controlling these insects. 


By 1982, 264 species and strains of parasites and predators were imported and released against 60 
species of introduced and native tree pests. In 1981, coccinellids were released in young cottonwood 
plantations in Mississippi to control the cottonwood leaf beetle (Solomon and Neel 1985; Neel and 
Solomon 1985). During the 1980s, Forest Service entomologists visited the People's Republic of 
China to identify natural enemies of "Asian" gypsy moth. They conducted preintroduction 
evaluations and developed a long-term project with Chinese scientists to identify alternate host 
requirements for maintaining parasite populations. Although parasite species from the China were 
sent to the United States, none were released. During this same period, a research program on natural 
enemies of exotic forest weeds in Hawaii was initiated and several foreign natural enemies were 
identified and released. Parasites of the larch casebearer continued to be released in the Northwest 
and survival was monitored for released parasites of both the larch casebearer in the Northwest and 
larch sawfly in the Northeast. Research was well underway to determine the effect of parasites and 
predators on the population dynamics of gypsy moth, Douglas-fir tussock moth, "eastern" and 
western spruce budworms, mountain pine beetle, and southern pine beetle. 


By the mid-1980s, nuclear polyhedrosis virus (NPV) sprays were developed in Canada for use 
against the European pine sawfly, Virginia pine sawfly, and Swaine jack pine sawfly, redheaded pine 
sawfly, forest tent caterpillar, European spruce sawfly, and other pests (Drooz 1985). A baculovirus 
production facility was established at the Forest Service Laboratory in Corvallis, OR, and used to 
produce viral insecticide for the Douglas-fir tussock moth. 


After termination of the accelerated gypsy moth research program, biological control research 
continued at the Northeastern Forest Experiment Station's research laboratories at Hamden, CT, 
Morgantown, WV, and Delaware, OH. Northeastern Area and Southern Region offices of Forest 
Health in West Virginia, New Hampshire, and North Carolina were responsible for the transferring 
of research technology through demonstrations and other applications of research. Southern pine 
beetle research continued at Pineville, LA. Spruce budworms research was conducted by units 
located in New England and the Pacific Northwest. 


104 | : 


Between 1980 and 1985, Forest Service CANUSA research on the "eastern" and western spruce 
budworms concentrated on the role of parasites, predators, antagonists, and pathogens in the 
population dynamics of the pests. In these studies, avian, arachnid, and formicid predators were 
found to be influential in regulating budworm populations. Inundative release of parasites were 
unsuccessful because the parasites failed to become established. Cooperators refined the application 
techniques and formulations of Br. A 1984 international symposium held in Bangor, ME, resulted in 
a summarization of the research results of Forest Service, state, and Canadian scientists. This 
information was used to develop management strategies for the budworms that integrated biological, 
chemical, and silvicultural control techniques (Sandors et al. 1985). 


Research on biological control of forest diseases focused on: 1) evaluating fungal interactions of 
Trichoderma spp. with Phellinus weirii and Armillaria spp.; 2) assessing the ability of hypovirulent 
isolates to control chestnut blight and other virulent cankers; and 3) the ability of Streptomyces spp. 
to control Dutch elm disease. Mycorrhizal fungi were identified and their host ranges, physiologies, 
and ecological diversities were assessed. Scientists at the Forest Products Laboratory evaluated 
Polyoxin D™ for control of wood-staining mold and decay fungi. 


Biological Control Activities, 1987-1993. By 1986, approximately 13% of the FIDR research budget 
was devoted to biological control research. This research effort was concentrated on insect pests 
(75%), tree diseases and wood decay (17%), and weed control (8%) (Stewart 1989). In October 1987, 
Forest Service project leaders met with the FIDR staff in Washington to discuss current and planned 
programs, and to identify priority areas for research. This information was used to develop a ten-year 
plan to guide FIDR into the twenty-first century, ensure that management decisions during the 1990s 
were consistent with national needs and priorities, and provide a framework for future planning. The 
plan released in August 1989 called for research focus on pests of national concern and on new 
research technologies. Centers would be developed for concentrated research to develop new 
technologies. This plan called for: 1) fundamental research to determine how interactions among 
hosts, pests, natural enemies, and the environment affected the frequency and severity of pest 
outbreaks; 2) operational research to develop effective and environmentally safe microbial agents for 
non-chemical control of insect and disease pests; and 3) the development of control tactics using 
parasites and predators either through inundative or augmentative releases. 


Research on interactions among plant hosts, pests, natural enemies, and the environment was located 
in Lincoln, NE (Rocky Mountain Forest and Range Experiment Station (RM)), Pineville, LA 
(Southern Forest Experiment Station (SO)), and Corvallis, OR (Pacific Northwest Forest and Range 
Experiment Station (PNW)). Development of effective and environmentally safe microbial agents 
was concentrated at Hamden, CT (Northeastern Forest Experiment Station (NE)), Delaware, OH 
(NE), East Lansing, MI (North Central Forest Experiment Station (NC)), and Corvallis, OR (PNW). 
Research to develop suppression tactics with parasites was concentrated in Hamden, CT (NE), 
Pineville, LA (SO), Corvallis, OR (PNW), and Hawaii (Pacific Southwest Forest and Range 
Experiment Station (PSW)). 


In 1988, a strategic plan on "Forest Health Through Silvicultural and Integrated Pest Management" 
was developed by WO staffs in response to congressional concern about the continued impacts of 
gypsy moth, southern pine beetle, mountain pine beetle, spruce budworms, root diseases, and 
atmospheric deposition on forest health. Congress also was concerned about the balance between 
short-term, commodity-oriented pest suppression projects and long-term investment in prevention 
and research. This plan decentralized Forest Pest Management Regional Offices, increased the 
number of regional offices (8 to 18) and established 27 new permanent positions nationwide. A 
cooperative Forest Health Monitoring Program was established by the Forest Service and the 
Environmental Protection Agency. WO Forest Pest Management also allowed the Forest Service to 


105 


continue production of Gypchek™, a biological insecticide for gypsy moth, until it could be 
produced commercially. 


In 1990, Congress amended the Cooperative Forestry Assistance Act of 1978 and strengthened the 
Forest Service programs concerned with forest health monitoring, technology development, and 
promotion of management measures to protect forest health. The strategic plan, "Healthy Forests for 
America's Future", was developed by the Forest Service in 1993 to further strengthen Forest Service 
policies and direction for responding to forest health problems. This plan updated and superseded the 
1988 plan. The strategic plan emphasized ecosystem management in the National Forests and 
integration of forest pest management into ecosystem management. It addressed congressional 
concern about forests where ecological conditions have been altered, resulting in increased 
susceptibility to drought, pest epidemics, wildfire, and introduced pests (USDA Forest Service 
1993a). The plan called for increases in biological control research: 1) to understand impacts of 
natural enemies on the population dynamics of pests in order to develop pest models and decision 
support systems needed to assist land managers in making management decisions; 2) to fill gaps in 
environmental data for Bt, increase research on the development of other key microbes, and assess 
the impacts of pesticides and microbes on non-target insects in the ecosystem; 3) to explore the use 
of classical biological control and conservation and enhancement of native controls and resistant 
varieties of trees in cooperation with other USDA agencies; and 4) to understand the ecological roles 
of forest insect pests, their natural controls, and other associated arthropods and microorganisms. 


In 1992, the USDA Forest Service Quarantine Laboratory was established in Ansonia, CT, to 
facilitate and accelerate research and development in biological control. This 3100 ft facility is 
certified to confine and colonize entomophagous and phytophagous arthropods and entomopathogens 
for biological control research. From 1992-93, research has focused on biological control of exotic 
pests. The facility management is designed for cooperative research with state, federal and 
international biological control projects. 


A "National Center for Forest Health Management" was established in Morgantown, WV, in April, 
1993, to: 1) facilitate the promotion, development, and use of technologies to sustain or enhance 
forest health, and 2) advance understanding of forest health and effects of forest health technologies 
on forest ecosystems management goals (USDA Forest Service 1993 b and c). Biological control 
efforts could include the introduction of exotic predators, parasites or pathogens, and/or 
augmentation of natural enemies; conservation or enhancement of native species; and evaluation of 
impacts of microbials and other pesticides on non-target species such as parasites, predators, or their 
alternative hosts. In 1993, the National Center for Forest Health funded research to evaluate the 
impacts of Bt, Dimilin™ and defoliation on non-targets, spread of the gypsy moth fungus, 
Entomophaga maimaiga, in the southern Appalachians, and formulation of the Gypchek™ virus for 
control of gypsy moth (USDA Forest Service 1993d). 


As the world economy becomes more global with goods and products traded among countries, the 
opportunities for the introduction of exotic pests increase. For example, concern about the 
importation of exotic pests has increased following the importation of gypsy moths in 1990 on birch 
logs imported from Russia, and the introduction in 1991, 1992 and 1993 via Germany to North 
Carolina of the "Asian" gypsy moth, "common pine shoot beetle", and an Eurasian poplar leaf rust. 
The spread of previously introduced European gypsy moth and white pine blister rust has increased 
this concern. Future research and survey efforts will focus on identification of biological control 
agents for these pests, and the development of biological control technologies needed to suppress and 
manage pest populations. 


In 1990, Forest Pest Management (Forest Health), International Forestry's Tropical Forestry Program, 
the International Institute of Biological Control (I[BC) in Great Britian, World Bank, United Nations 


106 


Development Program (UNDP) and the United Nations! Food and Agriculture Organization (FAO) 
initiated a cooperative project with Kenya's Forestry Department to identify potential parasites and 
predators of the "cypress aphid", Cinara cupressi, an aphid pest of tropical cypress in East Africa. 
This aphid was discovered in Malawi in 1986 and was found doing damage in Kenya in 1991. 


Biological control research and application highlights (Table 3) between 1986 and 1993 include: 1) 
completing research on the biological control of larch casebearer, one of the most successful and well 
documented cases of biological control in the Forest Service; 2) releasing of an exotic beetle predator 
(Rhizophagus grandis) of black turpentine beetle in the south; 3) release of natural enemies of 
several exotic weeds in Hawaii; 4) identifying potential predators of forest pests in forests, 
plantations, agroforestry systems and other plantings; 5) developing models that explain the role of 
natural enemies in regulating abundance of the spruce budworms, larch casebearer, and gypsy moth; 
6) commercially producing the microbials Gypchek™ (for gypsy moth) and BioControl-1™ (for 
Douglas-fir tussock moth); and 7) identifying new microbials and evaluating their effects on pest 
populations. Forest disease activities include: 1) assessing commercial Trichoderma spp. 
preparations against wood decay; and 2) evaluating Ophiostoma sp. for control of oak wilt, and 
Fusarium spp. for control of pitch canker on Virginia pine, and Steptomyces spp. to control poplar 
leaf spot and canker pathogens. 


Summary. Biological control activities within the Forest Service have increased as concern over 
chemical pesticide contamination of the environment and pest resistance to these chemicals has 
increased. Prior to the early 1970s, efforts were directed toward identification and release of 
parasites and application of chemical pesticides. During the 1970s and 1980s, research and 
application efforts focused on specific pests and were usually directed toward nonbiological control 
methods and the use of Bt and NPV. Biological efforts focused on use of these microbials and 
understanding the role of natural enemies in regulating abundance of gypsy moth, spruce budworms, 
and Douglas-fir tussock moth. During this time, research on biological control of forest diseases was 
minimal. Since 1986, public and administrative interest in biological control have increased, 
particularly during the 1990s. Research and application activities have focused on: 1) understanding 
the role of natural enemies in the ecosystem and development of methods to manipulate the 
ecosystems to enhance natural enemy effectiveness and survival; 2) developing more effective 
microbial insecticides and delivery systems and understanding their impacts on non-target organisms; 
and 3) identifying and releasing natural enemies that can be used to control exotic and native pests 
within the United States and other countries. Future development and implementation of biological 
control techniques will depend upon public acceptance of the long-term manipulation of ecosystems, 
concern over pesticide contaminants, and the availability of adequate levels of long-term funding 
needed to develop and implement biological control techniques. 


Acknowledgments. Special thanks are given to all who helped research and produce this overview 
and the detailed history in Appendix III: Frances Barney for her diligent efforts to obtain hard to find 
publications and information; Jennifer Irwin for her assistance in identifying, obtaining and recording 
the cited publications; Jane Deger, Chris Hopson, LeAnne Gustafson, and Marcia Gustafson for their 
help in locating publications. Numerous people reviewed parts of the manuscript, including Carol 
Schumann, Ned Klopfenstein, Tom ODell, Don Kinn, Dan Jennings, Lane Eskew, Arnold Drooz, 
Torolf Torgersen, Richard Reardon, and Gerard Hertel. Sylvia Christensen, Eleanor Oler, Jennifer 
Lindgren, and Michael Barnhart are acknowledged for their assistance in typing parts of the 
manuscript. 


107 


Table 3. USDA, Forest Service Research and Application Activities in Biological Control 


(1953-1993) 


[See Appendix III for additional information. ] 


Pest 


BARK BEETLES 
Black Turpentine Beetle 


Douglas-fir Beetle 


Spruce Beetle 


Mountain Pine Beetle 


108 


Years 


1953-1959 
1960-1969 
1970-1979 


1980-1986 
1987-1993 


1953-1959 


1960-1969 


1970-1979 
1980-1986 
1987-1993 
1953-1959 
1960-1969 


1970-1979 


1980-1986 
1987-1993 
1953-1959 
1960-1969 


1970-1979 


Activities 


* Identification of nematodes, clerids, mites and 
other natural enemies in the South. 

* Evaluation of their impacts. 

* Identification of exotic predators. 

* Release of the beetle predator, Rhizophagus 
grandis, in Louisiana. 

* Identification of nematodes and parasites in the 
Northwest. 

* Documentation of the biology and embryology of 
Coeloides brunneri. 

* Identification of arthropod parasites and 
nematodes, and avian predators. 

* Assessment of the impact of woodpeckers. 

* Assessment of the impacts of woodpeckers. 


* Identification of parasites in Colorado. 

* Identification, impact, and abundance of avian 
predators. 

* Evaluation of impacts of stand densities on 
woodpecker predation. 

* Identification of prey preference of woodpeckers. 


* Identification and evaluation of avian predators. 
* Identification of avian predators, and arthropod 
parasites and predators. 

* Identification of predatory mites. 

* Assessment of relative abundance and 
effectiveness of parasites and predators. 

* Publication of a "Key to Common Parasites and 
Predators." 

* Assessment of natural enemies’ responses to 
pheromones. 


Table 3. USDA, Forest Service Research and Application Activities in Biological Control 


(1953-1993) 


[See Appendix III for additional information. ] 


Pest 


Smaller European Elm 
Bark Beetle 


Southern Pine Beetle 


Miscellaneous Bark Beetles 


Years 


1980-1986 


1987-1993 


1953-1959 
1960-1969 


1970-1979 


1980-1986 
1987-1993 
1953-1959 
1960-1969 


1970-1979 


1980-1986 


1987-1993 


1953-1959 


1960-1969 


Activities 


* Assessment of relative abundance and 
effectiveness of predators. 

* Assessment of natural enemies responses to 
pheromones. 


* Importation of parasites from France. 

* Mass production and release of the parasite 

Dendrosoter protuberans. 

* Refinement of rearing techniques, and mass 
production and release of D. protuberans. 

* Evaluation of the population dynamics of D. 
protuberans. 


* Nematodes sprayed on infested trees. 

* Identification of parasites, predators, and 
associates. 

* Congress approves funding for Expanded 
Southern Pine Beetle Research and Application 
Program. 

* Identification, and determination of biologies and 
impacts of parasites and predators. 

* Determination of effects of selected natural 
enemies on population dynamics. 

* Handbook published on "How to identify common 
insect associates of the southern pine beetle." 

* Techniques developed for identifying previous 
hosts of natural enemies. 

* Assessment of the relative abundance and 
effectiveness of predators. 

* Evaluation of abundance patterns of natural 
enemies during outbreaks. 

* Identification of nematode parasites and 
determination of their distributions. 

* Identification of nematode parasites, mites and 
avian predators of the mountain pine beetle and 
nematodes of other bark beetles. 


Continued 


109 


Table 3. USDA, Forest Service Research and Application Activities in Biological Control 


(1953-1993)--Continued 


[See Appendix III for additional information. ] 


Pest 


HOOT B R 


Years 


1970-1979 


1980-1986 
1987-1993 


1953-1959 


1960-1969 


1970-1979 


1980-1986 


1987-1993 


HARDWOOD DEFOLIATORS 


Cottonwood Leaf Beetle 
and Other Chrysomelid 
Beetles 


Elm Spanworm 


110 


1953-1959 
1960-1969 
1970-1979 
1980-1986 


1987-1993 


1953-1959 
1960-1969 


1970-1979 


Activities 


* Identification of avian predators of spruce bark 
beetles and nematode parasites of bark beetles. 

* Ecological studies on nematode parasites of Ips 
spp. 

* Identification of native parasites of Rhyacionia 
spp. and exotic parasites of R. buoliana. 

* Identification of parasites of the egg, larvae and 
pupae of R. frustrana in the Southeast. 

* Ttoplectis quadricingulata, an exotic parasite of R. 
buoliana reared by scientists at Corvallis, OR. 

* Identification of parasites reared from Rhyacionia 
spp., needleminers and other Tortricidae throughout 
the U.S. 

* [. quadricingulata released against R. buoliana in 
Oregon. 

* Identification of parasites of Retinia metallica in 
the Great Plains and Rhyacionia zozana in the West 
and determination of their relative abundance. 

* Identification of parasites and predators of R. 
metallica in the Great Plains. 

* Determination of the impact of natural enemies on 
the population dynamics of R. metallica in 
Nebraska. 


<= 


* Augmentative release of Coleomegilla maculata in 
Mississippi. 

* Augmentative release of C. maculata in 
Mississippi. 

* Assessment of activity of Br isolates and their 
physiological interactions with cottonwood leaf 
beetles. 

* Research initiated to understand mechanism of 
resistance of the beetles to Bt. 

* Egg parasites cause the collapse of an outbreak in 
Southeast. 

* Identification of additional egg parasites and 
development of techniques for mass rearing them. 


Table 3. USDA, Forest Service Research and Application Activities in Biological Control 


(1953-1993) 


[See Appendix III for additional information. ] 


Pest Years 


1980-1986 
1987-1993 
Fall Cankerworm 1953-1959 
1960-1969 
1970-1979 


1980-1986 
1987-1993 
Gypsy Moth 1953-1959 
1960-1969 


1970-1979 


Activities 


* Survey of egg masses for parasites. 

* Survey of egg masses for parasites. 

* Identification of alternate hosts of Telenomus 
alsophilae and characterization of its biology. 

* Development of techniques for storage of host 
eggs and mass production of T. alsophilae. 

* Release of 7. alsophilae in Colombia to control 
Oxydia trychiata on Cupressus lusitanica and its 
successful establishment on O. trychiata. 


* Determination of parasite biologies and impacts. 
* Inundative release of Cotesia melanoscelus. 

* Cooperating P.L. 480 scientists in Spain, 
Yugoslavia, and India survey for natural enemies. 
* Evaluation of effectiveness of arthropod natural 
enemies, a nuclear polyhedrosis virus (NPV), and 
Bt. 

* Congress approves funding for the Expanded 
Gypsy Moth Research and Application Program. 

* Evaluation of effectiveness of parasites with 
Intensive Plot System. 

* Laboratory and field evaluation of Blepharipa 
pratensis. 

* Augmentative release of B. pratensis and 
inundative releases of 3 parasites with Br. 

* Demonstration that C. melanoscelus can transmit 
gypsy moth NPV. 

* Pre-introduction evaluations of potential exotic 
parasites. 

* Scientists visit the USSR to identify parasites and 
understand IPM practices. 

* Registration of Gypchek™, 

* Evaluation of Bt strains, formulations, dosages and 
physical properties. 

* Evaluation of spray droplet size and coverage for 
aerial and ground application. 


Continued 


111 


Table 3. USDA, Forest Service Research and Application Activities in Biological Control 


(1953-1993)--Continued 


[See Appendix III for additional information. ] 


Pest 


Miscellaneous Hardwood 


Nha ie 


Defoliators 


Years 


1980-1986 


1987-1993 


1953-1959 
1960-1969 


1970-1979 


1980-1986 


1987-1993 


Activities 


* Scientists visit the Peoples' Republic of China to 
identify natural enemies and conduct pre- 
introduction evaluations. 

* Development of joint long-term research projects 
with China on significance of alternative hosts for 
maintaining parasite populations. 

* Establishment of Gypsy Moth Research and 
Development Program and an extramural research 
program to develop methods to evaluate impact of 
parasites on gypsy moth population dynamics. 

* Research to develop an easy-to-use formulation of 
Gypchek™, 

* Initiation of research to quantify interactions 
between NPV and Nosema spp. and Vairimorpha 
spp. 

* Transfer of Entomophaga maimaiga into 
Michigan and the Southeast and initiation of E. 
maimaiga impact study on non-target insects. 

* Development of life system model with a 
predator/parasite submodel. 

* Development of methods to produce NPV in cell 
culture. 

* Evaluation of Br formulations, dosages and 
impacts on non-target arthropods. 


* Demonstration of effectivenesss of aerial 
application of Bt for cankerworm control in North 
Dakota. 

* Identification and documentation of aspects of the 
biology of Malachius ulkei, an egg predator of 
spring cankerworm in the northern Great Plains. 

* Assessment of impact of natural enemies on the 
abundance of a sawfly (Pontania sp. nr. pacifica) on 
willow in Arizona. 

* Assessment of effectiveness of Br against large 
aspen tortrix in Alaska. 


Table 3. USDA, Forest Service Research and Application Activities in Biological Control 


(1953-1993) 


[See Appendix III for additional information. ] 


Pest Years 


CONIFER DEFOLIATORS 

Blackheaded Pine Sawfly 1953-1959 
1960-1969 
1970-1979 


1980-1986 
1987-1993 
Douglas-fir Tussock Moth 1953-1959 
1969-1969 


1970-1979 


1980-1986 


1987-1993 


Activities 


* Identification and evaluation of the impact of 
parasites along the Gulf Coast. 
* Identification of parasites and fungi in Belize. 


* Identification of viruses. 

* Identification of viruses. 

* Pilot tests on control with viruses. 

* Control trials with NPV and Br. 

* Use of parasite abundance in egg masses to predict 
subsequent defoliation. 

* Congress approves funding for the Expanded 
Douglas-fir Tussock Moth Research and 
Application Program. 

* Identification and impacts of predators and 
parasites. 

* Keys to parasites and predators. 

* Distribution, impact, behavior of Telenomus 
californicus, an egg parasite. 

* Development of a viral insecticide by identifying 
and characterizing strains, testing potency, 
standardization and formulation trials, mammalian 
and fish toxicity and pathogenicity tests, etc., and 
propagation of the virus. 

* Registration of BioControl-1™ in 1976, the first 
virus registered in the U.S. for forest insects. 

* Pilot control study with NPV and Bz. 

* Evaluation of Bt strains, formulations, dosages, 
and physical properties. 

* Evaluation of spray equipment, droplet size, and 
coverage for aerial and ground application. 

* Identification of hymenopterous parasites and 
avian, arachnid, and insect predators. 

* Assessment of natural enemy impact on the moth. 
* Baculovirus production facility established at 
Corvallis, OR. 


Continued 


113 


Table 3. USDA, Forest Service Research and Application Activities in Biological Control 


(1953-1993)--Continued 


[See Appendix III for additional information. ] 


Pest 


Introduced Pine Sawfly 


Larch Casebearer 


Larch Sawfly 


Virginia Pine Sawfly 


114 


Years 


1953-1959 
1960-1969 
1970-1979 


1980-1986 


1987-1993 
1953-1959 


1960-1969 


1970-1979 


1980-1986 


1987-1993 
1953-1959 


1960-1969 
1970-1979 


1980-1986 


1987-1993 
1953-1959 
1960-1969 
1970-1979 


1980-1986 
1987-1993 


Activities 


* Survey for parasites in North Carolina. 

* Release of Monodontomerus dentipes, Exenterus 
amictorius, and Dahlbominus fuscipennis for 
control. 

* Release of M. dentipes for control. 

* Release of the egg parasites Dipriocampe diprioni, 
Chrysonotomyia ruforum and C. formosa in North 
Carolina in 1982. 

* M. dentipes continues to control the sawfly. 

* Canadian scientists develop life tables for 
parasites. 

* Collection of Agathis pumila in northeastern U.S., 
and rearing and release of the parasite in the 
Northwest. 

* Release of four species of parasites found in 
northeastern U.S. and two European parasites in the 
Pacific Northwest. 

* Evaluation of single-species vs. multi-species 
releases. 

* Releases of parasites in Pacific Northwest. 

* Evaluation of impacts of parasites on population 
dynamics. 

* Evaluation of impacts of parasites on populations. 
* Evaluation of distribution and impact of parasites 
in Minnesota. 

* Release and establishment of Olesicampe 
benefactor in Pennsylvania. 

* Evaluation of 0. benefactor survival in 
Pennsylvania. 


* Release of Monodontomerus dentipes, Exenterus 
amictorius, and Dahlbominus fuscipennis in 
Virginia. 


Table 3. USDA, Forest Service Research and Application Activities in Biological Control 


(1953-1993) 


[See Appendix III for additional information. ] 
Pest Years 
Redheaded Pine Sawfly 1953-1959 
1960-1969 
1970-1979 
1980-1986 
1987-1993 
Spruce Budworms and 1953-1959 


Jack Pine Budworm 
1960-1969 


1970-1979 


1980-1986 


1987-1993 


Activities 


* Release of Exenterus amictorius and Dahlbominus 
fuscipennis in North Carolina in 1969. 
* NPV used to control the sawfly. 


* Identification of natural enemies of spruce 
budworms in the northeastern and northwestern U.S. 
* Identification of predators, parasites, and 
pathogens of spruce budworms. 

* Documentation of spruce budworm biologies. 

* Assessment of avian predator impact on jack pine 
budworm abundance in Minnesota. 

* Identification of natural control agents and 
evaluation of their impacts and abundance. 

* CANUSA approved by Congress in 1977. 

* Evaluation of the effects of parasites and predators 
on the population dynamics of spruce budworm. 

* Pilot study evaluating spruce budworm control 
with Bt and NPV. 

* Evaluation of Bt strains, formulations, dosages, 
and physical properties. 

* Evaluation of spray equipment, droplet size, and 
coverage for aerial and ground application. 

* Evaluation of the impact of Nosema fumiferanae 
on population dynamics of spruce budworm. 

* Evaluation of the effects of parasites and predators 
on the population dynamics of spruce budworm. 

* Pilot tests evaluating the efficacy of Br. 

* Successful rearing of five generations of the 
parasite Glypta fumiferanae in California. 

* Release of the egg parasite Trichogramma 
minutum. 

* Assessment of parasite distribution. 

* Efficacy and field persistance of Bt after ground 
and aerial application on fir in Wisconsin. 

* Continuation of research to evaluate the impact of 
N. fumiferanae on budworms. 


Continued 


115 


Table 3. USDA, Forest Service Research and Application Activities in Biological Control 


(1953-1993)--Continued 


[See Appendix III for additional information. ] 


Pest 


Miscellaneous Conifer 
Defoliators 


SAP SUCKING INSECTS 
Balsam Woolly Adelgid 


MISCELLANEOUS 
INSECT PESTS 


FOREST DISEASES 
Root and Butt Rots 


116 


Years 


1953-1959 


1960-1969 


1970-1979 


1980-1986 
1987-1993 


1953-1959 


1960-1969 


1970-1979 
1980-1986 
1987-1993 
1953-1959 


1960-1969 
1970-1979 


1980-1986 


1987-1993 


1953-1959 
1960-1969 


1970-1979 


Activities 


* Evaluation of western hemlock looper control with 
Bt. 

* Assessment of effectiveness of aerial application 
of Bt against the pine butterfly. 


* Identification of natural enemies in Japan, India, 
and Pakistan. 

* Introduction of invertebrate predators. 

* Identification of predators in India and China (P.L. 
480). 

* Introduction of predators from India, Pakistan, 
England, Australia, Germany, Austria into New 
England, North Carolina, Washington, and Oregon. 


* Publication of list identifying and describing the 
biologies of parasites reared from microlepidoptera 
between 1915 and 1959. 

* Identification of spiders found in forest 
ecosystems, plantations, and other plantings. 

* Identification of parasites and predators of "striped 
pine scale" and "loblolly pine mealybug." 

* Identification of spiders found in forest 
ecosystems, plantations and other plantings. 

* Identification of spiders found in forests, 
plantations, and other plantings. 

* Identification of pathogens and parasites of stored 
products pests. 


* Development of methods for assaying soil for 
antagonistic organisms. 

* Evaluation of nematodes for control of Armillaria 
spp. 





Table 3. USDA, Forest Service Research and Application Activities in Biological Control 


(1953-1993) 


[See Appendix III for additional information. ] 


Pest 


Stem Cankers and Other 
Canker Diseases 


Mycorrhizal Symbiosis 


Years 


1980-1986 


1987-1993 


1953-1959 
1960-1969 
1970-1979 
1980-1986 


1987-1993 


1953-1959 


1960-1969 


1970-1979 


Activities 


* Evaluation of interactions of Trichoderma spp. 
with Phellinus weirii and Armillaria spp. 

* Evaluation of interactions of Trichoderma spp. 
with Phellinus weirii and Armillaria spp. 

* Evaluation of seed treatments with beneficials and 
antagonistic organisms for control of damping off 
and root rots of pines. 


* Impact of hypovirulent strains of Cryphonectria 
parasitica on chestnut blight. 

* Identification and impact of hyperparasite. 

* Impact of hypovirulence of C. parasitica on 
chestnut blight. 

* Evaluation of the ability of hypovirulent isolates 
to control virulent cankers. 

* Evaluation of Arthrobacter sp. and Fusarium sp. 
for control of pitch canker on Virginia and slash 
pine. 

* Evaluation of Streptomyces spp. for control of 
poplar leaf spot and canker pathogens. 

* Identification and isolation of ectomycorrhizal 
fungi. 

* Description of ectomycorrhizae of Douglas-fir and 
pine seedlings. 

* Identification and isolation of ectomycorrhizal 
fungi. 

* Host/fungus index developed for ectomycorrhizal 
fungi. 

* Development of practical inoculation procedures 
for nursery seedlings. 

* Development of a commercial source of Pisolithus 
tinctorius inoculum. 

* Isolation and confirmation of ectomycorrhizal host 
range. 

* Publication of a Monograph on Endogonaceae. 

* Evaluation of the influences of soil factors and 
natural disturbances on ectomycorrhizal fungi 
development on Douglas-fir, larch, and pines. 

* Evaluation of physiology and ecological diversity. 


Continued 


117 


Table 3. USDA, Forest Service Research and Application Activities in Biological Control 


(1953-1993)--Continued 


[See Appendix III for additional information. ] 


Pest 


Vascular Wilts 
agents. 


Wood Products 


118 


Years 


1980-1986 


1987-1993 
1953-1959 


1960-1969 
1970-1979 
1980-1986 


1987-1993 


1953-1959 


1960-1969 


1970-1979 


1980-1986 


1987-1993 


Activities 


* Isolation and confirmation of ectomycorrhizal host 
range. 

* Inoculation program with basidiospores. 

* Evaluation of physiology and ecological diversity. 


* Identification of potential biological control 


* Assessment of Streptomyces spp. for control of 
Dutch elm disease. 

* Evaluation of interactions of xylem-colonizing 
Bacillus spp. with verticillium wilt of maples. 

* Identification of bacterial and fungal endophytes 
of American elm. 

* Evaluation of Bacillus spp. and Pseudomonas spp. 
as biological controls of oak wilt. 

* Evaluation of colonization by Ophiostoma sp. for 
control of oak wilt. 

* Evaluation of enhancement of Trichoderma, 
growth, and reduced decay by treating pulpwood 
with fluoride. 

* Assessment of the impact of isolates of 
Trichoderma viride on Gloeophyllum sepiarium, 
and G. trabeum. 

* Evaluation of Polyoxin D™ for control of wood- 
staining mold and decay fungi. 

* Evaluation of antagonistic abilities of Gliocladium 
virens and various Trichoderma spp. against white 
and brown rot. 

* Assessment of potential Trichoderma spp. 
preparations and application of commercial 
Trichoderma spp. preparations against wood decay 
fungi. 

* Evaluation of interactive effect and persistence of 
Trichoderma spp. strains against wood decay. 

* Identification of additional antagonistic fungi. 

* Evaluation of the efficacy of bacteria against 
wood decay. 





Table 3. USDA, Forest Service Research and Application Activities in Biological Control 


(1953-1993) 


[See Appendix III for additional information. ] 


Pest Years 


WEEDS 1953-1959 
1960-1969 


1970-1979 


1980-1986 


1987-1993 


Activities 


-——- 


* Identification of fungi and insects associated with 
dwarf mistletoes and documentation of their 
biologies. 

* Evaluation of fungal distribution, host preferences, 
and impact. 

* Identification of fungi and insects associated with 
dwarf mistletoes and documentation of their 
biologies. 

* Evaluation of fungal distribution, host preferences, 
and impact. 

* Identification and release of exotic natural 
enemies of weeds in Hawaii. 

* Identification and release of eight exotic natural 
enemies of weeds in Hawaii. 


Li9 


CHAPTER VI 
1971-1993 
ANIMAL AND PLANT HEALTH INSPECTION SERVICE. 
Edited by W. C. Kauffman 


Biological control activities in the Animal and Plant Health Inspection Service (APHIS) are 
conducted in three work units: 1) Biological Control Operations, Plant Protection and Quarantine 
(PPQ); 2) Methods Development, PPQ; and 3) the National Biological Control Institute. Many of the 
biological control projects are conducted cooperatively between Biological Control Operations and 
Methods Development. Some of the projects discussed in this chapter will continue beyond the 1993 
cutoff date of this history. (As elsewhere in this history, full scientific names of all organisms 
mentioned in this chapter are given, and are cross-referenced, in the Appendix.) 


A. BIOLOGICAL CONTROL OPERATIONS, PLANT PROTECTION AND QUARANTINE. By 
D. E. Meyerdirk, G. L. Cunningham, T. L. Burger, and L. E. Wendel 


The Biological Control Operations (BCO) within the U. S. Department of Agriculture (USDA), 
Animal and Plant Health Inspection Service, had its origin in 1966 with the initiation of an 
operational program addressing the biological control of the cereal leaf beetle under the North 
Central Region of Plant Protection and Quarantine. Throughout the 1970s, biological control 
activities within APHIS were generally restricted to major quarantine pests such as cereal leaf beetle, 
gypsy moth, and citrus blackfly. Some of these activities were conducted, prior to the formation of 
APHIS, by the ARS Plant Protection Division (PPD), which was to become PPQ of APHIS, as 
discussed in Chapter IV, Section B.1.a. These programs were centered around production and 
large-scale redistribution of natural enemies. Viewed as highly successful and necessary (USDA 
1976b), these implementation procedures were suggested for use against additional pests. Practical 
application of biological control agents on a large-scale basis was recognized as a proper function of 
action agencies such as APHIS. APHIS, in cooperation with state departments of agriculture, 
provided leadership to exploit and expedite the use of proven natural enemies. 


The present goal of BCO within APHIS is "to implement biological control technologies to control 
agricultural pests of economic importance in a cooperative effort with federal and state agencies." 
The principal objective of the program is to mass produce and release native and exotic biological 
control agents for the control of selected arthropod and weed pests of agriculture. The effects of 
natural enemies on target pests is fostered through various activities, including: foreign collection, 
importation, quarantine screening, rearing, establishment, augmentative releases, and domestic 
collection and redistribution of the natural enemies. The first two tasks are generally conducted in 
close association with the Agricultural Research Service (ARS) and other research units. Surveys are 
conducted to confirm establishment and geographic distribution of selected natural enemies. Detailed 
evaluations of the effects of natural enemies on their target pests are conducted. Economic 
evaluations are conducted to determine the cost:benefit of each project, when possible. 


120 


1. Gypsy Moth (1963-1979) and Cereal Leaf Beetle (1966-1979) Programs 


Personnel at Otis Air Force Base, MA, have been involved in the collection, culture, and release of 
imported gypsy moth parasites since 1963 (see Chapter IV). In late 1971, these activities at Otis (now 
under PPQ) were discontinued and PPQ initiated the Gypsy Moth Parasite Distribution Program. 
Through cooperative agreements with the New Jersey Department of Agriculture, the University of 
Maryland, and later the Maryland Department of Agriculture, gypsy moth parasite rearing activities 
were continued. Parasites imported by ARS were mass-reared and made available for release in states 
which were newly infested or threatened by invasion by the gypsy moth. (Reardon et al. 1973; 
Reardon 1981; Reardon and Coulson 1981; Coulson 1981d.) 


The program against the cereal leaf beetle (CLB) was one of the most successful examples of 
classical biological control in the United States (Anonymous 1978; Graham 1984; DeBach and 
Rosen 1991). The beetle was first discovered in Michigan in 1962 and became a major pest of small 
grain crops, such as wheat, oats, and barley. The pest reduced yield up to 50% in some instances 
(Pierce 1982). A foreign exploration and importation program against the CLB was conducted by the 
Entomology Research Division of ARS. This was closely followed by a large-scale production and 
distribution program conducted by the Plant Protection Division (PPD) of ARS, in cooperation with 
Purdue and Michigan State Universities (see Chapter III, Section A.1.a). A laboratory was 
established by PPD for this program in Niles, MI; this became a PPQ facility after PPQ's creation in 
1971, now called the Niles Biological Control Laboratory. Four species of parasites (see Table 4) 
were imported from Europe. An egg parasite, Anaphes flavipes, proved very effective, along with 
three other species, which were larval parasites. An economic evaluation of the CLB program 
showed benefits ranged from $7 to $105 million annually (Moffitt et al. 1993). Total benefits (above 
costs) of the program were estimated at about $170 million, with benefit to cost ratio of 12:1. The 
program ended in 1979 after 13 years of cooperative efforts with state departments of agriculture, 
ARS, and many universities. Distribution of CLB during the 1970-1979 period was confined to the 
northeastern region of the U.S. Later, as the beetle invaded new areas, the program was resumed (see 
below). 


2. Initiation and Development of the PPQ Biological Control Implementation Program (1980-1993) 


APHIS-PPQ biological control implementation activities began in 1980, when PPQ significantly 
expanded its activities in biological control. The publication "Guidelines for PPQ Action Programs in 
Biological Control" was issued to define PPQ's roles and responsibilities (USDA 1980b). APHIS 
initiated biological control implementation projects by following the identification of specific 
agricultural pests on which sufficient research had been conducted to allow implementation of the 
research results. G. L. Cunningham was named Biological Control Staff Officer on PPQ's National 
Program Planning Staff, a position he occupied until 1990. During those ten years, a variety of 
actions were taken in support of biological control. A four-state, cooperative demonstration program 
for biological control of the Mexican bean beetle was conducted. A biological control 
implementation program against the alfalfa weevil was initiated in midwestern U.S. Construction was 
initiated for a biological control laboratory at Moore Field in Mission, TX (1980), now called the 
Mission Biological Control Laboratory. A satellite laboratory to the Mission facility was established 
in Bozeman, MT, in 1986 to provide assistance to a biological control of rangeland weeds program. 


A major revision of the BCO Program took place as a result of a review in 1985, and agency 
"guidelines" were revised. In 1986, D. E. Meyerdirk, joined the PPQ Operational Support Staff as a 
biological control technical specialist to implement the recommendations of the 1985 review. Since 
1990, he has served as the Chief of BCO in PPQ. A second BCO program review occurred in 1987. 
This review suggested that APHIS increase its leadership in biological control within the federal 
government. Specific responsibilities for APHIS-PPQ biological control were identified, as well as 


121 


other responsibilities shared jointly by APHIS and ARS. Basic functions in biological control 
programs were identified and the agency (APHIS or ARS) that was to have the lead role in each 
function was specified. The need to coordinate biological control research and implementation 
among USDA agencies led to the formation of the USDA Interagency Biological Control 
Coordinating Committee (IBC*) in 1988. This committee initially consisted of representatives from 
ARS and APHIS, but later included members from USDA's Forest Service, Extension Service, and 
Cooperative State Research Service as well (see also Chapter IV, Section A). 


In 1989, the National Biological Control Institute (NBCI) was established within APHIS, one 
purpose of which was to further coordination. This Institute is headed by E. S. Delfosse (see this 
Chapter, Section C). 


Following are brief summaries of biological control implementation programs targeting agricultural 
pests by APHIS-PPQ from 1980 to 1994. The natural enemies employed in these programs are listed 
in Table 4. 


Mexican bean beetle (1980-1984). The Mexican bean beetle program was a state/federal project to 
demonstrate the augmentative use of parasites. Building on previous activities against this pest in 
New Jersey, Maryland, Delaware, and Virginia, the project used the Indian eulophid parasite, 
Pediobius foveolatus, in the four-state area to demonstrate the effect of properly timed releases of 
parasites for control of the Mexican bean beetle (MBB). Since P. foveolatus does not overwinter in 
the U.S., laboratory-reared parasites were released in "nurse" plots, which consisted of plantings of 
early season snap beans, a preferred host of MBB. These nurse plots provided an early-season release 
and breeding site for parasites, which promoted establishment and increase in parasite numbers. As 
beetle populations increased in adjacent soybean fields, the parasites spread from the nurse plots to 
the soybeans. In soybeans, the parasites provided good control of the MBB and often eliminated the 
need for insecticides. The results of a large-scale biological and economic study of the project are 
available for use by other interested states and farm communities as an alternative control technology 
(Reichelderfer 1979; Dively 1985). (For early ARS involvement in the MBB program, see Chapters 
III and IV, above.) 


Alfalfa weevil (1980-1991). The alfalfa weevil biological control project was directed by the Niles, 
MI, laboratory, under the leadership of T. L. Burger. This program was an outstanding example of 
what can be accomplished when research and action agencies work together. Ten species of natural 
enemies were involved in the combined USDA program, as listed in Table 4 (Bryan et al. 1993). Five 
of these parasites (Bathyplectes anurus, B. curculionis, Microctonus aethiopoides, M. colesi, and 
Oomyzus [previously Tetrastichus] incertus) were shown by ARS and APHIS to be effective against 
the weevil (Dysart and Day 1976; Day 1981; Kingsley et al. 1993). In the 1950s and 1960s, these 
parasites were introduced and established by ARS in the northeastern U.S. (see Chapters III and IV). 
Weevil numbers were reduced and application of chemical insecticides for control of the weevil 
decreased by 73% by 1980. This saved alfalfa producers an average of $8 million a year in pesticide 
and application costs. In New Jersey alone, ARS estimated that the percentage of alfalfa fields 
treated for the pest decreased from 96% before parasite introductions to only 7% subsequently. 


Continued distribution of parasites to other states was considered by ARS to be beyond their primary 
mission. Consequently, in 1980, APHIS assumed responsibility for parasite distribution to new areas. 
Under APHIS direction, the program expanded from 17 northeastern states to all remaining portions 
of the continental U.S. Not all species became established in all states. Problems were encountered 
because additional U.S. strains of the alfalfa weevil and other species of related weevils were found 
in the western U.S. 


122 


During this program, more than 16 million parasites were released at 41,200 sites throughout the U.S. 
Seventy-three new state and 11,330 new county parasite-occurrence records were established as part 
of the program's biological evaluation studies (Bryan et al. 1993). The net social benefits of 
biological control of the alfalfa weevil has been estimated at $2.2 billion (Moffitt et al. 1990); see 
Section B of this Chapter for more detailed explanation of this economic analysis. 


Citrus whitefly (1981-1985). Biological control of citrus whitefly was begun in 1981 as a regional 
implementation project, and was directed by the new APHIS-PPQ Biological Control Laboratory at 
Mission, TX, under the leadership of L. E. Wendel. The objective of the project was to redistribute 
an introduced parasite, Encarsia lahorensis, throughout the southeastern states. This Asian parasite 
of citrus whitefly had been successfully established by university researchers in California and 
Florida, where it had successfully reduced citrus whitefly populations on citrus and ornamental 
plants (Nguyen et al. 1983). Nursery stock was infested with parasitized citrus whitefly produced in 
the laboratory at Mission and distributed to locations from Texas throughout the southeastern U.S. It 
is believed that the parasite has effected some control of citrus whitefly in the new areas where 
parasites are now established. The project has not yet undergone a detailed evaluation. 


Silverleaf nightshade (1982-1986). In 1982, the agency began a 5-year pilot project directed against 


the perennial weed silverleaf nightshade. This is an important weed in the southwestern U.S., 
infesting pastures, cotton, and other crops. An alternative to cultivation and application of herbicides 
is the use of a leaf-galling nematode, Ditylenchus (previously Orrina) phyllobius. The biological 
control of silverleaf nightshade project developed technology for large-scale augmentative use of the 
nematode. This native nematode causes extensive galling to the leaves, stems, and flowers of 
silverleaf nightshade. Infected plants are severely stunted and weakened. Techniques were developed 
to mass rear the nematode in field plots and to apply the inoculum at desired rates over broad 
infestations. Although effective in reducing silverleaf nightshade populations, the cost of producing 
the nematode was not competitive with use of herbicides. 


- . In 1985, APHIS began a project against the Colorado potato 
beetle (CPB). The goal of the project was to demonstrate the use of biological control agents as a 
component of an integrated pest management system for CPB. To accomplish this, APHIS 
collaborated with university, state, and federal (Methods Development Centers and ARS) 
cooperators. The Mission Biological Control Laboratory provided biological control agents and 
participated in laboratory and field studies, including studies on optimum release strategies for the 
agents, development of synthetic CPB diet, improvement of parasite and predator rearing methods, 
quality assessment of the natural enemies, economic evaluation, and development of public 
awareness programs for CPB biological control. APHIS also supported foreign exploration to search 
for new exotic agents. Natural enemies involved in this program are listed in Table 4. 


- . In 1985, the agency initiated cooperative biological 
control projects on diffuse and spotted knapweeds. This project was conducted by the APHIS 
laboratory at Mission, TX, and satellite facility at Bozeman, MT, in cooperation with ARS and 
university researchers in the northwestern U.S. The Bozeman facility was under the direction of 
R. D. Richard. Eight European insect species that had been approved for introduction into North 
America by U.S. and Canadian authorities were obtained for distribution either from North American 
establishment sites or directly from overseas laboratories of ARS and the International Institute of 
Biological Control (IIBC) (Table 4). Some of these agents have become established and are 
spreading. Weed biological control offers ranchers solutions that are long-term and considerably 
more cost effective when compared to other means of control. (For ARS research on the biological 
control agents for these weeds, see Chapter IV, Section C.) 


123 


European corn borer (1986-1993). The European corn borer (ECB) has a host range which includes 
over 200 plants, among which are corn, snap beans, sorghum, cotton, peppers, and apples. A 
cooperative survey was initiated in 1986 to identify existing natural enemies attacking ECB eggs or 
larvae in the U.S. A specific objective was to determine the distribution of Lydella thompsoni, a 
European dipterous parasite, reintroduced from Delaware to additional areas. A total of 73,192 ECB 
larvae from 1,337 collection sites in 28 states were processed at the APHIS laboratory in Mission, 
TX. Two additional, previously-introduced European parasites were recovered during the collections 
(Eriborus terebrans and Macrocentrus grandii) as well as three pathogens (Bacillus thuringiensis, 
Beauveria bassiana, and Nosema pyrausta). Collaborators have also provided exotic egg parasites 
from China (Zrichogramma dendrolimi and T. ostriniae) and a larval parasite from Egypt 
(Habrobracon brevicornis). Some of the natural enemies listed in Table 4 were used to develop 
integrated pest management programs for ECB and/or released for establishment purposes. 


Aphids (1987-1988). Biological control of aphids began as a project in 1987 with the redistribution 
of the sevenspotted lady beetle, Coccinella septempunctata, throughout the U.S. This European lady 
beetle was first found in New Jersey long after initial introduction attempts by ARS (see Chapters III 
and IV), and soon became the dominant aphid predator in portions of the eastern U.S. APHIS and 
state cooperators determined the U.S. distribution of the beetle, established field collection sites, and 
collected and redistributed the species across the western third of the country. This program was later 
redirected toward a newly introduced aphid pest, the Russian wheat aphid (see below). 


Leafy spurge (1988-present). Leafy spurge is a major rangeland weed infesting millions of acres of 
grazing land in the western U.S. and Canada. In 1988, Congress directed APHIS to implement 
biological control of leafy spurge as part of a pest management approach. The work was done 
together with state, ARS, and Canadian scientists who had previously identified, studied, and 
obtained release authorization for several exotic natural enemies of the weed (see Chapter IV, 
Section C). The APHIS laboratory in Mission, TX, and its satellite facility at Bozeman, MT, 
determined the extent of leafy spurge infestations, supported foreign collection of the natural 
enemies, and assisted in their quarantine screening, establishment, and redistribution. In addition, 
economic and biological evaluations were conducted. Initial efforts concentrated on releasing four 
chrysomelid flea beetles, Aphthona cyparissiae, A. nigriscutus, A. czwalinae, A. flava; a cecidomyiid 
midge, Spurgia esulae; and a cerambycid beetle, Oberea erythrocephala (Table 4). 


Russian wheat aphid (1988-1993). Using funds previously devoted to the aphid biological control 
program, APHIS developed a comprehensive biological control program against the Russian wheat 
aphid (RWA). This pest invaded the U.S. from Mexico in 1986 and has caused up to a 70% reduction 
in yield in small grains. This aphid is a major problem to grain growers in the western half of the 
US. The project initially focused on importing exotic parasites and predators by ARS and university 
reseachers. Parasite rearing facilities to support the project were developed at the Biological Control 
Laboratory in Mission, TX, in association with Texas A & M University. Exotic predators and 
parasites (Table 4) were reared at APHIS laboratories at Mission, TX, and Niles, MI, with overall 
project leadership at the Niles laboratory. 


Biological control was one of several components in a RWA integrated pest management system. 
APHIS worked with the National Association of State Departments of Agriculture and other interest 


groups to coordinate their biological control efforts with other control efforts (Anonymous 1989, 
1990, 1991). 


Euonymus scale (1991-1993). The euonymus scale occurs throughout most of the U.S. attacking 
ornamental species of euonymus. It is a serious economic pest to the nursery industry, affecting 
landscape plants in both commercial and residential areas. ARS imported several natural enemies 
from South Korea (see Chapter IV), including the predators Chilocorus kuwanae and Cybocephalus 


124 


sp. prob. nipponicus (Table 4). These were established and found to control the euonymus scale 
effectively. In addition, two parasite species were introduced from China by university cooperators 
(see Table 4). In 1991, BCO began implementation of the euonymus scale biological control project. 
Through cooperative efforts, the success of the project is being measured by the reduction of scale on 
euonymus by these exotic natural enemies. 


Sweetpotato whitefly (1991-1993). The sweetpotato whitefly was recognized as a serious economic 
threat to agriculture in the U.S. in 1981, when the whitefly was found attacking field and vegetable 
crops in the farming areas of the desert Southwest (Arizona and southern California) (Meyerdirk et 
al. 1986). In the late 1980s, a new "biotype" or "strain" of the whitefly was found severely attacking 
poinsettias and vegetables across the southern U.S. This new pest was causing silverleaf disease of 
squash and irregular ripening of tomatoes. Through an USDA Interagency Cooperative Agreement, 
APHIS began the development of a biological control program against this pest as part of an 
integrated pest management program. The APHIS Mission, TX, laboratory is conducting quarantine 
screening of exotic natural enemies from Europe, the Middle East, and Asia, that have been collected 
by ARS, IIBC, and university scientists. Most of the parasites were species of Encarsia or 
Eretmocerus (see Table 4). 


Cereal leaf beetle (1993). In 1993, APHIS reestablished a cereal leaf beetle (CLB) biological control 
program, which was originally begun in 1966 (see above). This action was taken because the CLB 
expanded its geographical distribution after 1979 from the northeastern and midwestern U.S. into 
Utah, Montana, and Idaho. The natural enemy complex that successfully controlled the CLB in the 
Northeast and Midwest did not move naturally with the pest to these new areas. In addition, the CLB 
in the southeastern portion of its range (North and South Carolina, Georgia, and Alabama) was not 
effectively controlled by the existing natural enemy complex. The latter may have been the result of 
the failure of the previously imported natural enemies to acclimatize in the Southeast. ARS is 
presently (1994) conducting foreign collection of known and new CLB natural enemies from more 
southern climatic zones of Europe for the APHIS program. These will be released in the southeastern 
and western U.S. Previously established CLB parasites will also be collected in the northeastern and 
midwestern U.S. for redistribution in the West. 


B. METHODS DEVELOPMENT, PLANT PROTECTION AND QUARANTINE. By W. C. 
Kauffman and P. C. Kingsley 


1. History of Methods Development 


Methods Development, as a specific activity identified in the U.S. Department of Agriculture 
(USDA), began in the 1930s as part of the Bureau of Entomology and Plant Quarantine. Much of the 
early work was carried out by the Aircraft and Special Equipment Center in Greenfield, MA, which 
provided technical support (i.e., services and aerial application activities) to USDA projects. In the 
mid-1940s, a laboratory was established at Hoboken, NJ, to develop commodity treatment schedules 
for the use of methyl bromide, ethylene dibromide, and cold treatments. During the 1950s and 1960s, 
other laboratories were created to investigate control techniques for various pests such as boll weevil, 
gypsy moth, cereal leaf beetle, imported fire ants, pink bollworm, and witchweed. These laboratories 
were under the administrative control of the USDA regions in which they were located. In 1969, the 
Plant Protection Division of the USDA Agricultural Research Service (ARS) was reorganized, and a 
new Branch, called Methods Development, was created. The mission of this Branch was to fulfill the 
growing need for a specific group to work with the research community to develop practical pest 
control by transferring small-scale tests into pilot programs and full-scale operational technologies. 
Specific responsibilities of these Methods Development facilities were: 1) involvement in 
cooperative efforts with research agencies to ensure that plant pest control needs were addressed, and 
2) development of large-scale eradication programs in pilot trials. A Chief Staff Officer was assigned 


125 


to supervise the activities of the following Methods Development facilities and one Equipment 
Center: 
Boll Weevil Methods Development Laboratory, Gulfport, MS; 
Cereal Leaf Beetle Methods Development Laboratory, Niles, MI; 
Cereal Leaf Beetle Parasite Rearing Laboratory, Niles, MI; 
Gypsy Moth Methods Development Laboratory, Otis Air Force Base, MA; 
Hoboken Methods Development Laboratory, Hoboken, NJ; 
Imported Fire Ant Methods Development Laboratory, Gulfport, MS; 
Pink Bollworm Methods Development Laboratory, Brownsville, TX; 
Pink Bollworm Moth Rearing Facility, Phoenix, AZ; 
Witchweed Methods Development Laboratory, Whiteville, NC; and 
Methods Development Equipment Center, Beltsville, MD. 


In 1971, the Animal and Plant Health Inspection service (APHIS) was established as a separate 
agency of the USDA with responsibility for Plant Protection and Quarantine (PPQ) operational 
programs. Methods Development Centers were placed in APHIS and their mission was to provide the 
agency with scientific and technological capabilities for protecting and improving American 
agriculture and public health. Methods Development continues to support APHIS programs primarily 
by optimizing existing pest control practices and by developing new technologies for pest exclusion, 
detection, and control. This is accomplished by developing and refining methods for controlling plant 
pests, evaluating new biological and chemical materials, adapting or inventing equipment, providing 
technical consultation and training, collecting and disseminating pertinent information, participating 
in strategic and tactical planning, serving as a liaison between APHIS and the research community, 
and integrating technological advancements into pest management systems. 


These activities are performed at the following five centers: 

Hoboken Methods Development Center, Hoboken, NJ; 

Mission Methods Development Center, Edinburgh, TX (moved in 1983 from the Brownsville 
Methods Development Center, Brownsville, TX. Field Stations: Gainesville, FL; 
Guatemala City, Guatemala; State College, MS; Waimanalo, HI); 

Otis Methods Development Center, Otis Air Force Base, MA; 

Phoenix Methods Development Center, Phoenix, AZ (established 1989. Field Station: 
Brawley, California); 

Whiteville Methods Development Center, Whiteville, NC (Field Stations: Little Rock 
[Dillon], SC; Gulfport, MS). 


2. Biological Control Activities 


Methods Development Centers have contributed significantly to the development and success of 
many biological control activities of APHIS, as described below. Many of these projects involved 
close cooperation between the Centers and the Biological Control Operations (BCO) laboratories 
(Niles, MI, and Mission, TX). Further details on implementation of these biological control projects 
are described in Section A of this Chapter. 


Gypsy Moth Biological Control (1963-1993) - Otis Methods Development Center. The early work 
with gypsy moth parasites at Otis AFB under ARS' Plant Protection Division is noted in Section A.1. 
Work on other gypsy moth natural enemies was also conducted at Otis and continued after 
establishment of APHIS-PPQ in 1971. 


a) Bacillus thuringiensis Strains and Formulations (1963-1993). Work conducted at the Otis Center 
has been instrumental in the testing, development and registration of B. thuringiensis (Bt) for use as 


an effective material to control gypsy moth. For the past 30 years, Bt strains and formulations have 


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been tested in the laboratory and effective strains and formulations have been tested in the field using 
aerial application. These tests led to the registration of most of the Bt formulations presently used for 
gypsy moth control. Field testing led to the development of a higher dosage, single application 
technique now used, compared to previous double applications at low dosage. Also, the majority of 
data on weather effects on Bt efficacy, including the first field testing, was developed at the Otis 
Center. "Stickers" were tested and recommended for use with each Bt formulation. Otis personnel 
continue to test new strains and formulations of Br in laboratory bioassays on oak seedlings and to 
conduct field studies with Bt for improvement of its efficacy and safety to the environment. 


b) Nuclear Polyhedrosis Virus (1963-1993). From 1963-1965, personnel at the Otis Center first 
collected, purified, and applied nuclear polyhedrosis virus (NPV) from field-collected gypsy moth 
larvae. In the 1970s, following development of gypsy moth mass rearing techniques and an artificial 
diet, Otis personnel provided gypsy moth eggs and larvae to the Forest Service for the production of 
NPV (Podgwaite 1981). From 1977-1982, a pilot production team of ARS and APHIS scientists 
harvested NPV from cadavers of infected larvae reared at Otis (Shapiro 1981). On several occasions, 
egg masses were supplied to private industry in attempts to produce virus for purification by the 
Forest Service. Since these attempts were unsuccessful, the Otis Center has continued to collaborate 
with the Forest Service to produce cadavers (up to 7.5 million per year) for NPV production (1987- 
1993). Efforts continue to transfer NPV rearing technology to private industry in North America. 


c) Ceranthia samarensis (1992-1993). Improvements for the rearing of this European tachinid 
parasite are underway in collaboration with Forestry Canada. This parasite is associated with low- 
density populations of gypsy moth larvae in Europe. This effort involves improvements to Forestry 
Canada's rearing method. The feasibility of artificially implanting parasite maggots onto host larvae 
is being tested. Preliminary results indicate that artificial implantation can be used to propagate the 
parasite in the laboratory; however only maggots with highly developed mandibles successfully 
parasitize gypsy moth larvae. Further refinements of both methods are needed to increase rearing 
efficiency to assist a cooperative USDA and Forestry Canada project of C. samarensis release and 
establishment in North America. 


- - Missi Vv . In 1974, parasites of the citrus 
blackfly were taken from Mexico to Brownville, TX, where colonization methods were developed. 
Subsequently, these parasites were released in south Texas and were monitored for establishment. 
Surveys in Texas later recovered four parasite species: Encarsia opulenta, E. clypealis, E. smithi and 
Amitus hesperidum. From 1976-1980, E. opulenta and A. hesperidum were mass reared using 
hydroponically-fed, potted, rough-lemon plants as hosts for the citrus blackfly, and were released in 
south Texas by Mission Center personnel and in south Florida by the Florida Division of Plant 
Industry. These two parasites became established in 1980 in south Florida where they dramatically 
reduced citrus blackfly populations (Nguyen et al. 1983). The State of Florida continues to rear these 
parasites for release. 


xican Bean le (1979-1984) - Mi 
BCO. Beginning in 1979, procedures were developed for mass rearing the Mexican bean beetle, a 
pest of green beans and soybeans, and its parasite Pediobius foveolatus. This parasite was released by 
BCO in several eastern and midwestern states. Methods Development personnel worked in Maryland 
to determine optimal parasite release rates for production in nurse plots, parasite dispersal from these 
plots, and level of control in green beans and soybeans (Mellors et al. 1983). By 1984, results from 
field studies in Maryland and Indiana indicated reductions in Mexican bean beetle populations. 


f; il (1981- - Otis Meth e Wi i . An alfalfa weevil 


biological control evaluation survey (1981-1989) was designed by ARS, APHIS, and Economic 
Research Service to document changes in alfalfa weevil populations due to the establishment of new 


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parasite species (Kingsley et al. 1993). This project was coordinated by the Otis Center in 
cooperation with the Niles BCO Laboratory. Biological and economic data were collected by 
APHIS-PPQ personnel from cooperating alfalfa growers in 180 alfalfa fields sampled in nine states 
for up to eight years. Results from this survey indicated that biological control was an important 
factor in maintaining alfalfa weevil populations below economic injury levels. Analysis of the 
economic data with an econometric model suggested that net social benefits to producers and 
consumers from the Alfalfa Weevil Biological Control Program were $2.2 billion for the duration of 
the project (White 1989; Moffitt et al. 1990). This amount is equivalent to a perpetual stream of net 
social benefits of $88 million per year measured in 1987 dollars. Net social benefit refers to the 
difference between estimated market benefit and government expenditures. The expected cost:benefit 
ratio associated with the biological program against the alfalfa weevil is 1:87. 


Hydrilla (1981-1993) - Whiteville Methods Development Center. When hydrilla was discovered in 
the All-American Canal in the Imperial Valley of California in 1979, this invasive alien aquatic weed 
was deemed to be a catastrophic threat to this irrigation system. Since APHIS is the agency that 
administers the Federal Noxious Weed Act, Methods Development joined in an interagency task 
force to examine potential controls. White amur, commonly referred to as the grass carp, provided 
efficient hydrilla control in the Imperial Valley. Mechanically-induced triploidy in this fish induced 
sterility, providing a non-reproducing biological control agent that has virtually eliminated hydrilla 
and other troublesome weeds from this irrigation system. The triploid white amur is now (1993) 
extensively used nationwide for aquatic weed management. 


Citrus Whitefly (1982-1983) - Mission Methods Development Center, with Mission BCO. Initial 
work was done on mass rearing the citrus whitefly and its parasite, Encarsia lahorensis. 
Improvements in whitefly rearing included the use of a non-citrus host (viburnum). These 
improvements in rearing enabled BCO to produce adequate numbers of parasites for field release. 


Silverleaf Nightshade (1982-1984) - Mission Methods Development Center, with Mission BCO. A 
method was developed to disinfect seeds of silverleaf nightshade and other Solanum species for 
tissue culture studies. A method to extract and count the leaf-galling nematode, Ditylenchus (as 
Orrina) pyllobius, was also developed. Although D. pyllobius inoculum was effective against 
silverleaf nightshade, this project was terminated by BCO in 1986 due to the high cost of producing 
the inoculum. 


Sugarcane Borer and Mexican Rice Borer (1981-1991) - Mission Methods Development Center. 
Mass-rearing techniques were developed, at the request of the Rio Grande Valley Sugar Growers 
Association, for the sugarcane borer and the Mexican rice borer as hosts for the parasites Cotesia 
flavipes, Allorhogas pyralophagus and Rhaconotus roslinensis. Improvements in rearing included 
egg-disinfecting and antimicrobial agents, and the publication of a Standard Operating Procedure 
Manual (Martinez et al. 1988). This technology was transferred to the Texas A & M University 
Experiment Station for continued experimental work. 


Colorado Potato Beetle (1985-1993) - Otis and Mission Method Development Centers, with Mission 
BCO. An artificial diet was developed for Colorado potato beetle (CPB) adults as a host for the egg 
parasite Edovum puttleri. Adults were reared on the improved diet for up to eight generations with no 
loss in quality compared to beetles reared on potato foliage. The parasite completed its life cycle on 
eggs from diet-reared beetles. New methods were developed to increase the efficiency of rearing the 
parasite in the laboratory for release. The use of CPB eggs killed by irradiation eliminated 
cannibalism by larvae from unparasitized eggs. Methods were also developed for mass producing the 
coccinellid Coleomegilla maculata, an egg predator, on a diet of air-dried Mexican fruit fly eggs. 
Fecundity, larval survival, and developmental time were improved compared to the standard raw 


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pork liver diet. The BCO project using natural enemies in integrated pest management of the 
Colorado potato beetle is ongoing (1993). 


Aphid Biological Control (1987-1988) - Otis Methods Development Center, with Niles BCO. 
Beginning in 1987, APHIS-PPQ-BCO redistributed the introduced aphid predator Coccinella 
septempunctata in the U.S. in an effort to suppress pest aphids in agricultural habitats. Methods 
Development contributed to this rearing and release effort by improving mass rearing techniques. 
The nutritional suitability of several aphids for the predator's larvae and adults was determined 
through laboratory life table analysis, and it was recommended that pea aphid, rather than greenbug, 
be used as prey in mass rearing. 


The results of two field studies in Massachusetts demonstrated the ability of C. septempunctata to 
reduce field populations of aphids in small field cages and open field plots (Kauffman and Schwalbe 
1991). These studies indicated that field evaluations of natural enemies should strive to quantify 
plant growth and crop yield responses to reduced pest herbivory under biological control. 


The Otis Center, in cooperation with BCO and research cooperators in Arkansas, Kansas, and Texas, 
evaluated the ability of C. septempunctata and Hippodamia convergens, a native coccinellid, to 
suppress aphids in small grains and alfalfa. Despite apparent visual differences, high variability of 
aphid populations and small numbers of replications prevented any demonstration of statistically 
lower aphid densities in cages with coccinellids compared to controls. The two predators reduced 
aphids to a similar degree and had no obvious incompatibility with each other. 


Russian Wheat Aphi : - Oti h Vv n with Niles and Mission 
BCO. With the assistance of APHIS-PPQ field personnel and BCO, a field sampling method was 
developed for a national survey of Russian wheat aphid (RWA) and its natural enemies in the U.S. 
This sampling method employed visual sampling of plant tillers and sweep netting and was used to 
evaluate the impact of beneficial species on RWA populations. In addition, other techniques for 
evaluating the effects of natural enemies on RWA were developed during two years (1990-1992) of 
cooperative agreements between Otis Center and state cooperators in California, Colorado, Idaho, 
Kansas, and Texas. These included: 1) sampling techniques for RWA and its natural enemies, 2) 
insecticidal exclusion, 3) exclusion cages, 4) inclusion cages, 5) host exposure on single-plant 
exclusion cages, and 6) host plant assessments in surrounding non-agricultural habitats. These 
evaluation techniques included a standardized impact and economic evaluation work plan, 
coordinated by Methods Development and BCO with cooperators, for implementation in selected 
sites throughout the RWA distribution in the U.S. beginning in 1994. 


Because RWA usually feeds inside the sheaths of rolled leaves of susceptible grasses, a laboratory 
study determined to what extent coccinellids collected from RWA homelands were adapted to search 
for RWA prey inside rolled leaves. Among the predators, Scymnus frontalis was found to be better 
adapted than Hippodamia variegata, H. tredecimpunctata, and Propylea quatuordecimpunctata to 
exploit this "prey-protecting niche," and appeared to offer the greatest promise for RWA biological 
control in the U.S. (Kauffman and LaRoche 1994), 


Improved rearing techniques were developed for another aphidophagous predator, Leucopis ninae, 
which was reared and released by BCO against RWA. Findings from laboratory studies and from 
field studies done in cooperation with ARS suggested that RWA concealment in rolled leaves limited 
the effectiveness of L. ninae against RWA. 


Mexican Fruit Fly (1990-1 - Mission Meth velopm nter. Techniques were developed 
for mass rearing the larval parasite Diachasmimorpha longicaudata using irradiated Mexican fruit 
fly, i.e., larvae that pupate but do not produce adult flies. Releases were made into commercial citrus 


129 


and wild hosts in northern Mexico, and a recommendation was made to include the release of 
parasites as part of the future development of fly-free zones in that area. 


Investigations were conducted in 1993 to determine the effect of Bacillus thuringiensis isolates on 
Mexican fruit fly adults. Four active isolates were identified, and soil samples from Guatemala were 
collected to identify and culture additional Br strains. 


Euonymus Scale (1991-1993) - Otis Methods Development Center, with Niles BCO. The objectives 


of this project were to determine the impact of the euonymus scale on its host and to determine how 
the establishment of natural enemies affects scale populations and the survival of the euonymus host. © 
A survey to estimate the economic benefits of the Euonymus Scale Biological Control Program was 
developed in collaboration with BCO and the University of Massachusetts. The survey was 
implemented in eleven states in 1993 and is to continue through 1996. 


Sweetpotato Whitefly (1991-1993) - Phoenix Methods Development Center, with Mission BCO. 


Phoenix Center personnel have collaborated with ARS researchers at the Western Cotton Research 
Laboratory, Phoenix, AZ, in enhancing a method of mass rearing the native predator Geocoris 
punctipes using artificial diet (Cohen and Staten 1994). Trial releases were conducted in southeastern 
California and Arizona in early 1993. Preliminary data show that the predator feeds extensively on 
sweetpotato whitefly. Collaborative studies have also been initiated to devise rearing methods and 
study the feeding behavior of Catana parcesetosa, an exotic coccinellid predator of whiteflies. The 
Phoenix Center provided support for areawide whitefly management trials on cotton in three 
locations in southern Arizona and California in 1993. These trials incorporated inundative releases of 
Chrysoperla species to supplement naturally occurring biological control. 


Methods Development also stationed an entomologist in Brawley, CA, to evaluate exotic natural 
enemies released against the whitefly. Exotic parasites for the releases were produced at the Mission 
BCO Laboratory. This program involved: 1) pre-release surveys to document the indigenous natural 
enemies, 2) releasing and establishing exotic natural enemies, 3) surveys to demonstrate natural 
enemy recovery and dispersal, 4) population studies of whitefly and its enemies on major crops 
throughout the year, 5) field and laboratory evaluations of the efficacy of exotic and indigenous 
natural enemies and their impact on whitefly populations, and 6) providing voucher specimens for 
morphological and molecular taxonomic studies. 


Beauveria bassiana for Rangeland Grasshoppers (1991-1993) - Phoenix Methods Development 


Center. Formulations of this fungal pathogen were developed and tested in laboratory and small field 
tests against the complex of rangeland grasshoppers. Work in 1993 included a large-scale field test 
and examination of effects of the fungus on non-target organisms. 


3. Acknowledgements 


We thank Norm Leppla (Chief, Methods Development, APHIS, PPQ) for his guidance in 
development of this document, and the following persons from the Methods Development Centers 
who contributed information: Jim Brazzel, Danny Gates, Tom Forrester, and A. J. Martinez 
(Mission); Win McLane and John Tanner (Otis); Bob Staten, Kim Hoelmer, and Nick Colletto 
(Phoenix); and Bob Eplee and Randy Westbrooks (Whiteville). We are especially thankful to Danny 
Gates for the information on history of Methods Development. 


C. THE NATIONAL BIOLOGICAL CONTROL INSTITUTE. By E. S. Delfosse 


The National Biological Control Institute (NBCI) was established in 1990 by the Animal and Plant 
Health Inspection Service (APHIS) "to promote, facilitate, and provide leadership for biological 


130 





control". It is thus a unique group in the history of biological control in the United States. NBCI had 
a relatively short, but very intense, ontogeny. Some of the important steps in the formation of NBCI, 
as well as recent changes in its activities, are discussed below. 


1. Establishment of NBCI 


A chronology of significant events in establishment of NBCI is presented in Table 5. Several reviews 
of biological control policy and implementation in APHIS preceded establishment of NBCI. In 
October 1985, a Review Team headed by W. W. Metterhouse of the New Jersey Department of 
Agriculture submitted a "Biological Control Program Evaluation Report" (APHIS, PPQ 1985) to 
Harvey L. Ford, then Deputy Administrator of the Plant Protection and Quarantine (PPQ) unit. The 
terms of reference of this report are directly relevant to establishment of NBCI: 


"A. Review the established [PPQ] biological control goals, objectives, and 
guidelines, to update or modify them based on current needs. 

B. Review current procedures for selecting, developing, and implementing biological 
control projects. Determine if existing procedures are appropriate and, if not, modify 
them to improve program results. 

C. Review program activities at the Mission, Texas, and Niles, Michigan, 
laboratories to assess activities and accomplishments. Make recommendations on 
resource needs and other areas of concern. 

D. Review the existing organizational structure of biological control and the 
interrelationships between laboratory/staff personnel with the field organization. 
Make recommendations for increasing organizational effectiveness which will 
benefit PPQ and further the accomplishment of biological control objectives. 

E. Make recommendations on the future of the PPQ biological control program 
specifically addressing such items as funding, personnel, additional rearing facilities, 
etc. 

F. Determine whether an ARS employee should be stationed at the Mission 
Laboratory." 


There were 18 recommendations from the "Metterhouse Report," four of which are relevant to this 
discussion of NBCI: 


"4, Increase national visibility of the biological control program through aggressive 
public relations. 

6. Take the lead in establishing an interagency biological control advisory group 
within the USDA. 

11. Establish a Program Manager position at Hyattsville, Maryland, reporting to the 
Assistant Deputy Administrator for National Programs, to direct the overall 
biological control program. 

12. Establish a Biological Control Specialist position to provide technical and 
scientific expertise in program operation and development." 


Recommendations 4 and 6 were implemented by APHIS; 11 and 12 were deferred pending review of 
the National Program Planning Staff by a private contractor. 


The next pivotal document in the formation of NBCI is called the "Thomas Report" (APHIS 1987). It 


was commissioned by William F. Helms, Deputy Administrator, PPQ, in May 1987, and had the 
following terms of reference: 


I51 


"(Mr. Helms] asked PPDS to propose for top management consideration, the roles 
PPQ should play in the future to develop, implement and evaluate biological control 
projects. The new roles proposed should contribute to: (1) increasing the impact of 
biological control projects; and (2) increasing the involvement of other 
organizational entities." 


The recommendations of the Thomas Report were as follows: 


"This Committee recommends that PPQ take the leadership role in the United States 
for all aspects of biological control of pests of interest and high priority to the 
Agency and to American Agriculture. By doing so, the Agency will fill a void not 
currently addressed by any other organization. We recommend that PPQ take the 
leadership role by implementing and managing the 'Holistic Approach to Biological 
Control.’ ... In taking the lead, PPQ would identify and prioritize its own projects of 
interest; become involved in foreign exploration, quarantine operations, screening 
natural enemies, importation, colonization and establishment, evaluating 
effectiveness of natural enemies; and distributing natural enemies in large-scale 
implementation projects. In addition, PPQ would expand its role in developing 
augmentative biological control projects which could also complement Integrated 
Pest Management (IPM) programs conducted by the Agency." 


These recommendations were also accepted in principle by the then-Administrator, Donald L. 
Houston (Houston 1987), who, on December 21, 1987, suggested that the APHIS biological control 
activities should be developed in a "world recognized center of excellence for biological control". 
This is the first reference to developing NBCI as a center of excellence with a mandate beyond the 
USDA. 


Several drafts of a plan for a "National Biological Control Service Institute (NBCSI) within APHIS" 
were developed and discussed from 1987-89. Dr. Houston's successor, James W. Glosser, announced 
on March 22, 1989, at the Biological Control Centennial Celebration in Washington. that there would 
be anew APHIS initiative: the NBCSI. The aims of the NBCSI would be (Glosser 1989): 


"... to provide an expansion of implementation services, improved coordination, and 
a greater leadership role for APHIS in biological control. This initiative has been 
taken as a key strategy in protecting American agriculture through the use of 
environmentally sound methods. The initiative and the concept of the Institute is the 
result of an intensive series of meetings and reports involving APHIS staff and line 
managers over the past two years." 


In fact, there were prolonged and often spirited discussions between interested parties from 1986-88 
as to the NBCI location, mission, stakeholders, and related matters. Many locations within APHIS 
(an existing unit, or the Office of the Administrator), and outside APHIS (to somewhere in the 
Department of Agriculture, or becoming "independent"), were discussed. This culminated in an 
important Decision Paper in 1989 that concluded that the two most appropriate locations were PPQ 
and Science and Technology (S&T), and recommended that PPQ would be the most appropriate 
location. 


However, in the ensuing discussions, this position was reversed, and it was decided that S&T was the 
most appropriate initial location for NBCI. It was felt that an "institute" must be scientifically-based, 
and strategically-oriented. At least initially, NBCI would have a policy role, rather than a program 
role, and would be given a global orientation. This "noble" vision of NBCI was approved formally by 


132 


Dr. Glosser in 1990, and a "National Biological Control Institute Implementation Plan" (APHIS 
1990) was released on February 15, 1990. 


Thus, the formative period of NBCI, during which critical philosophical issues were examined in 
extreme detail, can be considered to be 1985-90. NBCI rose out of the perceived need for a biological 
control group that would be capable of interacting at all administrative and scientific levels, and 
would have a global focus. 


2. The Initial Mission, Functions and Staffing of NBCI 


The mission of NBCI is "to promote, facilitate, and provide leadership for biological control" 

(APHIS 1990). The initial NBCI functions (APHIS 1990) were to: 

™ ensure national leadership for the development and implementation of biological control; 

m™ develop an effective network of federal, state, and private organizations committed to biological 
control; 

= solicit input from cooperating institutions in identifying potential biological control projects; 

= identify and support the technical needs of cooperators and clients; collect, analyze, and 
disseminate general and technical information on biological control activities; 

™ expedite acquisition, development, and implementation of biological control agents; 

™ coordinate technical education and training programs; and 

™ integrate biological control with other pest management technologies. 


Other functions were to be added as biological control customers identified them. 


Six positions were approved initially for NBCI: Director, Secretary, Technical Coordinator, 
Technical Consultant, Database Manager, and Computer Operator. NBCI was committed to 
facilitating the use of the scientific and other expertise in the global community to the fullest extent 
in its operations. 


Additionally, a Visiting Scientist position was established, which was to be filled for relatively short 
periods of time by world-class scientists or other specialists. These individuals advise and consult on 
a relevant biological control problem, perform a specific function such as a review or a survey, etc. 
There have been two NBCI Visiting Scientists to date (1993): Dan Girling (University of Israel), who 
advised on biological control of whiteflies, and V. C. Moran (Dean of Science at Cape Town 
University), who advised on the international role of NBCI. 


The Director was to be "a world-class biological control scientist who must be capable of operating 
at all scientific, technical, social, environmental, media, legal and political levels." Entrepreneurial 
policy, media and educational campaigns would be necessary. It is essential that the Director 
maintain scientific credibility. The Director was to manage the budget and staff, and was to provide 
consultation to APHIS units and to the Administrator on biological control and related 
environmental, sustainable agriculture, and integrated pest management issues. 


To ensure that NBCI would continue to receive current, complete, and accurate details on operational 
and scientific needs, critical issues, and feedback on NBCI activities, a Customer Advisory Panel 
(CAP; formerly "User Advisory Panel") was established. On this Panel (Table 6) were 16 
outstanding individuals from federal and state governments, universities, and the private sector. CAP 
members serve three-year terms, and three members are replaced each year. CSRS Regional 
Biological Control Projects recommend their representative. The NBCI CAP is the only cross-cutting 
customer group in the U.S. to give consistent direction to a biological control/integrated pest 
management policy group, and has contributed significantly to the early success of NBCI. 


133 


In 1989, NBCI was formally named one of the three APHIS "Centers of Excellence." NBCI reported, 
for an interim period of February-March 1990, to the Director of S&T through the Director of 
Methods Development, and in March 1991, NBCI reported directly to the Director of S&T. In late 
1991, APHIS was reorganized, and S&T was disbanded. All locations in APHIS (and some outside 
of APHIS) were considered for NBCI. From this examination it was concluded that it would be 
inappropriate to place the NBCI in any APHIS Unit, because two insurmountable problems would be 
created: 1) a perception that the NBCI is less important to APHIS, and 2) a structural incompatibility. 
In regard to 1) the clear message to customers would be that NBCI was not considered as important 
to APHIS as it was when it was first established. This would make it difficult, if not impossible, for 
NBCI to achieve its mission. And in regard to 2), since all APHIS Units are important NBCI 
customers, it is clearly inappropriate for NBCI to be located in any of them. 


After considering all possible locations for NBCI, the Administrator decided in January 1992 to 

elevate NBCI to the Office of the APHIS Administrator. There are several benefits to this level of 

reporting, and no obvious disadvantages to NBCI. Some of the significant advantages are: 

= higher visibility within APHIS, which will lead naturally to higher visibility outside of APHIS; 

= astrong show of support for NBCI and its environmental activities; 

= easier access to and by the decision- and policy-makers; 

= ability to interact more easily with the Administrator and the APHIS Management Team (AMT) 
on critical issues facing biological control and integrated pest management. 


3. The Current Role of NBCI 


It was recognized from the outset that NBCI would be a special, "noble" effort by APHIS. It was to 
be a scientifically and philosophically based policy group, rather than an operationally oriented 
group, but would still have to operate effectively with line programs. Identifying customers, 
determining collaboratively their needs, and providing services is an important NBCI mandate. 


In effect, NBCI was established to be an entrepreneurial policy group for biological control, 
encouraged to interact freely within APHIS and other USDA agencies, universities, the National 
Plant Board, state departments of agriculture and similar bodies, special interest groups, the 
environmental community, industry, politicians, the media, the international community, etc. 


It was obvious that there was a need in the U.S. for such a group to act for biological control and 
integrated pest management, and that it could only do so if it were given an unusual amount of 
freedom, responsibility and accountability. This was particularly important because the NBCI was 
located within APHIS, and there was criticism that several of its key customers (in particular, 
Biotechnology, Biologics and Environmental Protection [BBEP], Biological Control Operations 
[BCO], and Biological Assessment and Taxonomic Support [BATS]) were also in APHIS. Despite 
having no line responsibilities for programs or regulations, it was important for NBCI to interact with 
these customers. 


NBCI currently (1993) has lead roles in biological control and integrated pest management policy, 
training and education, and facilitating biological control. For example, in early 1992, NBCI was 
charged by the APHIS Administrator with reviewing the APHIS biological control policy. This was 
undertaken in six steps: Examine APHIS legislative authority; develop a philosophy; confirm lines of 
authority; document current regulatory procedures; develop, with customers, new regulations and 
procedures; and enter into a process of renewing regulations and procedures regularly, with 
significant input from customers. 


This process took a year to complete. A highlight is the APHIS Biological Control Philosophy, 
approved by the then-Administrator, Robert B. Melland, on August 7, 1992. This philosophy states: 


134 


"APHIS believes that modern biological control, appropriately applied and 
monitored, is an environmentally safe and desirable form of long-term management 
of pest species. It is neither a panacea nor a solution for all pest problems. APHIS 
believes that biological control is preferable when applicable; however, we also 
recognize that biological control has limited application to emergency eradication 
programs. Whenever possible, biological control should replace chemical control as 
the base strategy for integrated pest management. 


"In support of this philosophy, APHIS will develop regulations that facilitate the 
release of safe biological control agents, while maintaining adequate protection for 
American agriculture and the environment. The regulations will give clear and 
appropriate guidance to permit applicants, including specific types of data needed for 
review and environmental analysis and specific time limits for Agency review. They 
will be updated as the science progresses. APHIS believes that public input on 
procedures to approve the release of biological control agents is a desirable and 
necessary step, and will strive to gather input from scientists, industry, and the 
public." 


Existing procedures for approval of biological control agents were examined, with input from APHIS 
(BATS and BBEP, primarily), and customers (scientists, environmental groups, commercial groups, 
and international groups). Input was also sought from these same groups for the elements needed to 
improve the procedures, and drafts of a new process were prepared. The final draft is currently being 
reviewed internally, and will be distributed for external comment via the Federal Register. 


NBCI is developing a training and education plan to help meet the needs of biological control. For 
example, NBCI is developing with collaborators a series of written and video materials that discuss 
biological control in a non-technical manner. Each 3-year age class from pre-school to university 
level will be covered. The first video, which addresses the mature, but scientifically-unsophisticated 
customer group, was (1993) in final production. An extensive computerized NBCI Bulletin Board 
System has been established and is used by the biological control community. A cooperative 
arrangement with the ARS Biological Control Documentation Center has been established to 
maximize the effectiveness of each group in delivering biological control information. 


NBCI's facilitation efforts have resulted in granting over $1 million since 1990 in funds for 
implementation evaluation of biological control, including support for meetings and publications. To 
address the critical shortage of systematists in groups of importance to biological control, NBCI has 
awarded three, 2-year Post-Doctoral Positions in Systematics. Two major Focus Group Workshops 
have been facilitated by NBCI: Scientific Considerations in Release of Transgenic Arthropod 
Biological Control Agents (with Marjorie A. Hoy of the University of Florida), November, 1993, and 
New Directions in Biological Control of the Gypsy Moth (with other USDA agencies, universities, 
and states), early January, 1994. Workshops on quarantine issues, documentation, host specificity, 
commercial biological control, and other issues are planned. 


4. Future of NBCI 


In three years, NBCI completed the primary goals for which it was established. A strategic planning 
process has continued. One outcome of this process is development of an NBCI Program Logic 
Model, philosophy, and vision for biological control. With customer input, these documents help 
frame the future activities of NBCI. 


135 


Clearly, biological control is becoming the method of choice for pest management around the world 
(for example, the current U.S. Administration is committed to increasing biological control as part of 
sustainable agriculture and integrated pest management). These sentiments mirror those of NBCI. 


However, biological control faces many critical scientific, legal, political and social issues, which are 
hindering severely the objective conception, development, and implementation of programs. The 
historical structure of science in general and biological control in particular in the U.S. has been 
incapable of addressing these issues effectively. Most university and government scientists are 
neither trained nor willing to deal with difficult legal, political, or social conundra. NBCI is a unique 
government body which was formed to deal with these difficult issues. NBCI is capable of 
continuing to serve agriculture and the environment in the United States and internationally, and with 
continued support, will meet this goal. 


136 


Table 4. Pests and Associated Natural Enemies for USDA Programs Coordinated by the 
Biological Control Laboratories of the Animal and Plant Health Inspection Service, Plant 
Protection and Quarantine 


Pest Natural Enemy 
Species Order:Family 
(Common Name) Species 
Order:Family 
PEST 
Bemisia tabaci (Gennadius) Hymenoptera: Aphelinidae 
(Sweetpotato whitefly) Encarsia formosa Gahan 
Homoptera: Aleyrodidae Encarsia lutea (Masi) 


Encarsia nigricephala Dozier 
Encarsia pergandiella Howard 
Encarsia transvena (Timberlake) 
Encarsia sp. nr. strenua (Silvestri) 
Encarsia spp. 
Eretmocerus mundus (Mercet) 
Eretmocerus spp. 
Coleoptera: Coccinellidae 
Catana parcesetosa (Sicard) 
Fungi 
* Beauveria bassiana (Bals.) 
*Paecilomyces spp. 


Dialeurodes citri (Ashmead) Hymenoptera: Aphelinidae 
(Citrus whitefly) Encarsia lahorensis (Howard) 
Homoptera: Aleyrodidae 


Diuraphis noxia (Mordvilko) Coleoptera: Coccinellidae 
(Russian wheat aphid) Adalia bipunctata (L.) 
Homoptera: Aphididae Coccinella septempunctata L. 
Coccinella transversoguttata graminum 
Mader 


Coccinellina ancoralis (Germar) 

Coleomegilla quadrifasciata 
(Schoenherr) 

Eriopis connexa Mulsant 

Hippodamia tredecimpunctata (L.) 

Hippodamia variegata (Goeze) 

Oenopia conglobata (L.) 

Propylea quatuordecimpunctata (L.) 

Scymnus frontalis Fabricius 

Semiadalia undecimnotata (Schneider) 


Continued 


137 


Table 4. Pests and Associated Natural Enemies for USDA Programs Coordinated by the 
Biological Control Laboratories of the Animal and Plant Health Inspection Service, Plant 
Protection and Quarantine--Continued 





Pest Natural Enemy 

Species Order:Family 
(Common Name) Species 
Order:Family 

Diuraphis noxia (Continued) Diptera: Chamaemyiidae 


Leucopis ninae (Tanasijtshuk) 
Diptera: Syrphidae 

Eupeodes nuda (L.) 

Sphaerophoria scripta (L.) 
Hymenoptera: Aphelinidae 

Aphelinus albipodus Hayat & Fatima 

Aphelinus asychis Walker 

Aphelinus varipes (Forster) 

Aphidius colemani Viereck 

Aphidius matricariae Haliday 

Aphidius picipes (Nees) 

Aphidius rhopalosiphi DeStefani-Perez 

* Aphidius uzbekistanicus Lushetzki 

Diaretiella rapae (M'Intosh) 

Ephedrus plagiator (Nees) 

Praon gallicum Stary 


Epilachna varivestis Mulsant Hymenoptera: Eulophidae 
(Mexican bean beetle) Pediobius foveolatus (Crawford) 
Coleoptera: Coccinellidae 


Hypera postica (Gyllenhal) Hymenoptera: Ichneumonidae 
(Alfalfa weevil) Bathyplectes anurus (Thomson) 
Coleoptera: Curculionidae Bathyplectes curculionis (Thomson) 


Bathyplectes stenostigma (Thomson) 
Hymenoptera: Pteromalidae 
Dibrachoides dynastes (Forster) 
Peridesmia discus (Walker) 
*Trichomalus inops (Walker) 
Hymenoptera: Braconidae 
Microctonus aethiopoides Loan 
Microctonus colesi Drea 
Microctonus stelleri Loan 
Hymenoptera: Eulophidae 
Necremnus leucarthros (Nees) 
Oomyzus incertus (Ratzeburg) 


138 


Table 4. Pests and Associated Natural Enemies for USDA Programs Coordinated by the 
Biological Control Laboratories of the Animal and Plant Health Inspection Service, Plant 


Protection and Quarantine 


Pest 


Species 
(Common Name) 
Order:Family 


Hypera postica (Continued) 


Leptinotarsa decemlineata (Say) 
(Colorado potato beetle) 
Coleoptera: Chrysomelidae 


Ostrinia nubilalis (Hiibner) 
(European corn borer) 
Lepidoptera: Pyralidae 


Natural Enemy 


Order:Family 
Species 


Hymenoptera: Mymaridae 
* Patasson luna (Girault) 


Hymenoptera: Eulophidae 
Edovum puttleri Grissell 
Diptera: Tachinidae 
Myiopharus doryphorae (Riley) 
Myiopharus sp. 
Coleoptera: Coccinellidae 
Coleomegilla maculata (DeGeer) 
Heteroptera: Pentatomidae 
Perillus bioculatus (Fabricius) 
Neuroptera: Chrysopidae 
*Chrysoperla rufilabris (Burmeister) 
Nematoda: Enoplida: Mermithidae 
Hexamermis sp. 
Nematoda: Rhabditida: Steinernematidae 
Steinernema feltiae (Filipjev, 1934) 
Bacteria 
* Bacillus thuringiensis sandiego 


Diptera: Tachinidae 
Lydella thompsoni Herting 
Hymenoptera: Braconidae 
Macrocentrus grandii Goidanich 
Macrocentrus linearis (Nees) 
Habrobracon brevicornis (Wesmael) 
Hymenoptera: Ichneumonidae . 
Eriborus terebrans (Gravenhorst) 
Hymenoptera: Trichogrammatidae 
*Trichogramma chilonis Ishii 
*Trichogramma dendrolimi Matsumura 
Trichogramma nubilale Ertle & Davis 
Trichogramma ostriniae Pang & Chen 
Bacteria 
* Bacillus thuringiensis Berliner 
Fungi 
* Beauveria bassiana (Bals.) 


Continued 


139 


Table 4. Pests and Associated Natural Enemies for USDA Programs Coordinated by the 
Biological Control Laboratories of the Animal and Plant Health Inspection Service, Plant 
Protection and Quarantine--Continued 


Pest Natural Enemy 

Species Order:Family 
(Common Name) Species 
Order:Family 

Ostrinia nubilalis (Continued) Protozoa 


* Nosema pyrausta (Paillot) 


Oulema melanopus (L.) Hymenoptera: Mymaridae 
(Cereal leaf beetle) Anaphes flavipes (Forster) 
Coleoptera: Chrysomelidae Hymenoptera: Ichneumonidae 


Diaparsis temporalis Horstmann 

Lemophagus curtus Townes 
Hymenoptera: Eulophidae 

Tetrastichus julis (Walker) 


Unaspis euonymi (Comstock) Coleoptera: Coccinellidae 
(Euonymus scale) Chilocorus kuwanae (Silvestri) 
Homoptera: Diaspididae Coleoptera: Nitidulidae 
Cybocephalus sp. prob. nipponicus 
Endrédy-Yonga 


Hymenoptera: Aphelinidae 
Coccobius sp. nr. fulvus 
(Compere & Annecke) 
Encarsia sp. nr. diaspidicola 
(Silvestri) 


WEED PESTS 
Centaurea diffusa Lam. Coleoptera: Curculionidae 
(Diffuse knapweed) Bangasternus fausti (Reitter) 
Centaurea maculosa Lam. Cyphocleonus achates (Fahraeus) 
(Spotted knapweed) Larinus minutus Gyllenhal 
Asterales: Asteraceae Coleoptera: Buprestidae 


Sphenoptera jugoslavica Obenberger 
Diptera: Tephritidae 

Chaetorellia acrolophi White & Marquart 

Terellia virens (Loew) 

Urophora affinis Frauenfeld 

Urophora quadrifasciata Meigen 
Lepidoptera: Gelechiidae 

Metzneria paucipunctella Zeller 
Lepidoptera: Pterolonchidae 

Pterolonche inspersa Staudinger 


140 


Table 4. Pests and Associated Natural Enemies for USDA Programs Coordinated by the 
Biological Control Laboratories of the Animal and Plant Health Inspection Service, Plant 


Protection and Quarantine 


Pest 


Species 
(Common Name) 
Order:Family 


Centaurea spp. (Continued) 


Euphorbia esula L. 


(Leafy spurge) 
Euphorbiales: Euphorbiaceae 


Solanum elaeagnifolium Cav. 
(Silverleaf nightshade) 
Solanales: Solanaceae 


Natural Enemy 


Order:Family 
Species 


Lepidoptera: Tortricidae 
Pelochrista medullana (Staudinger) 
Lepidoptera: Cochylidae 
Agapeta zoegana L. 
Acari: Acariformes: Eriophyidae 
*Aceria centaureae (Nalepa) 


Coleoptera:Chrysomelidae 
Aphthona cyparissiae (Koch) 
Aphthona czwalinae Weise 
Aphthona flava Guillebeau 
Aphthona lacertosa Rosenheim 
Aphthona nigriscutis Foudras 
Coleoptera: Cerambycidae 
Oberea erythrocephala (Schrank) 
Coleoptera: Curculionidae 
*Oxicesta geographica (Fabricius) 
Diptera: Cecidomyiidae 
Dasineura sp. nr. capsulae Kieffer 
*Spurgia capitigena (Bremi) 
Spurgia esulae Gagné 
Diptera: Anthomyiidae 
Pegomya curticornis (Stein) 
Pegomya euphorbiae (Kieffer) 
Pegomya transversaloides Schnabel 
Hymenoptera: Eurytomidae 
*Furytoma sp. 
Hyles euphorbiae (L.) 
Lepidoptera: Sesiidae 
Chamaesphecia crassicornis Bartel 
Chamaesphecia hungarica (Tomala) 
Lepidoptera: Noctuidae 
* Simyra dentinosa Freyer 
Fungi 
* Uromyces scutellatus (Pers.) Ler. 
* Uromyces striatus Schroet. 


Nematoda: Tylenchida: Anguinidae 
Ditylenchus phyllobius 
(Thorne) Filipjev 


ee 


* Natural enemies associated with cooperators, but not a direct responsibility of APHIS-PPQ-BCO. 


14] 


Table 5. Chronology of events leading to the establishment of the National Biological Control 


Institute in APHIS 





Date 


Item 





October 1985 


May 1987 


October 1987 


November 1987 


December 1987 


December 1987 


February 1988 


February 1988 


April 1988 


August 1988 


Dr. Harvey Ford, APHIS Administrator, established a review team, 
headed by Mr. William Metterhouse, to review APHIS biological 
control. A report entitled APHIS, PPQ Biological Control Evaluation 
Report was submitted, and circulated widely for comment. 


Mr. William Helms asked Program Planning and Development Staff 
(PPDS), PPQ, to determine if the roles being played by PPQ in 
biological control program were appropriate and what role PPQ should 
play in the future to develop, implement, and evaluate biological control 
projects. The "Thomas Committee," headed by Mr. Ed Thomas, 
established for this review. 


A Biological Control Review Report submitted by the Thomas 
Committee. 


Briefing paper submitted to the Administrator Office entitled Biological 
Control: A Recommendation, 1987. 


Biological Control Program Orientation and Recommendation made to 
Dr. Donald Houston, APHIS Administrator, which discussed the 
Thomas Report. 


Dr. Houston states that APHIS should upgrade its activities in biological 
control and should establish a "world recognized center of excellence," 
which became NBCI. 


Briefing paper Status of the New Biological Control Initiative in the 
Animal and Plant Health Inspection Service (APHIS) submitted to the 
Administrator, Dr. Jim Glosser. 


D. E. Meyerdirk presented APHIS' New Biological Control Initiative to 
the USDA, ARS Biological Control Matrix Team, and Delfosse. D. L. 
Husnik wrote E. B. Knipling, ARS, about the initiative. These efforts 
helped obtain intraagency support for NBCI. 


Position paper submitted to the Administrator's Office Proposed Animal 
and Plant Health Inspection Service (APHIS) Initiative in Biological 
Control. 


The New APHIS Biological Control Initiative and Task Element Matrix 
presented to Dr. Dean Plowman, ARS, by Dr. James Glosser. 


Table 5. Chronology of events leading to the establishment of the National Biological Control 
Institute in APHIS 


Date Item 

October 1988 APHIS Reorganization, creating a new Unit called Science and 
Technology. 

January-April 1989 Intense planning activities by APHIS, during which the formation of 
NBCI was debated. 

March 1989 Dr. Glosser announced of the New APHIS Biological Control Initiative 


and the Biological Control Institute presented during the Biological 
Control Centennial Celebration on the Patio of the Administration 


Building. 
March 1989 NBCI named as one of three APHIS "Centers of Excellence." 
April 1989 NBCI "Organizational Decisions" were identified: 1) What is the 


structure of the institute; 2) How would the institute be staffed; 3) To 
whom should the institute report. 


February 1990 National Biological Control Institute Implementation Plan released, and 
the search for the first Director begun. 


September 1991 Organizational Review by the APHIS Management Team decisions 
released. Decision Number 6 was: "Scientific support for line delivery 
units will be enhanced through re-integrating the Science and 
Technology unit's functions into the operational units with which they 
are primarily aligned. A Transition Team chaired by Dr. Charles 
Schwalbe has been charged to develop a comprehensive action plan for 
the orderly transfer of functions." 


January 1993 APHIS Administrator, Robert Melland, elevated NBCI to the Office of 
the Administrator. 





143 


Table 6. NBCI Customer Advisory Panel Members, 1990-92 








Name Organization Location Dates 
(Also Representing) 
Dr. W.L. Bruckart USDA, ARS, NAA Frederick, MD 1992-95 
Dr. G. Buckingham USDA, ARS Gainesville, FL 1993-96 
Dr. J.R. Cate USDA, CSRS Washington, DC 1990-94 
Dr. J.H. Frank Entomology & Nematology Dept. Gainesville, FL 1990-92 
University of Florida 
Mr. R.C. Frey Arizona Biological Control, Inc. Tucson, AZ 1990-92 
(Assoc.of Natural Bio-Control 
Producers) 
Mr. R. Gaskalla Florida Div. of Plant Industry Gainesville, FL 1992-96 
(National Plant Board; States) 
Dr. T.J. Kring University of Arkansas Fayetteville, AR 1990-92 
Dr. J.L. Krysan USDA, ARS, Natl. Progr. Staff Beltsville, MD 1993-96 
Dr. N.C. Leppla USDA, APHIS, PPQ, Methods Devel. Hyattsville, MD 1990-94 
Dr. R.F. Luck University of California Riverside, CA 1990-93 
Dr. J.V. Maddox Illinois Natural History Survey Champaign, IL 1992-96 
Dr. D.L. Mahr University of Wisconsin Madison, WI 1990-93 
Mr. W. Metterhouse New Jersey Dept. of Agr. Trenton, NJ 1990-92 
(National Plant Board; States) 
Dr. D.E. Meyerdirk USDA, APHIS, PPQ, BCO Hyattsville, MD 1990-94 
Mr. G. Scriven Biotactics (Assoc. of Natural Grand Terrace, CA 1992-96 
Biocontrol Producers) 
Dr. R.S. Soper USDA, ARS, OIRP Beltsville, MD 1990-92 


144 


EPILOGUE 


A. ACCOMPLISHMENTS AND CURRENT STATUS OF ARS RESEARCH ON CLASSICAL 
BIOLOGICAL CONTROL OF ARTHROPODS AND WEEDS. By J. R. Coulson, C. J. 
DeLoach, R. I. Carruthers, and K. J. Hackett 


As noted in Chapters III and IV, the Agricultural Research Service (ARS) classical biological control 
(CBC) programs, and the CBC programs of its predecessor Bureau of Entomology and Plant 
Quarantine (BEPQ; see Chapters I and II) have produced some very significant accomplishments, in 
terms of both research results and successful pest control over the past 110 years. This Epilogue does 
not purport to provide updated information on USDA biological control programs beyond the 
history’s cutoff date of December 1993. However, a number of important general biological control 
publications, in addition to those referenced above, can be reported here and are included in the 
Reference Cited section: National Research Council (1996); Van Driesche and Bellows (1996); 
Barbosa (1998); and Bellows and Fisher (1999). Also, a reference overlooked in preparing the 
history, Sawyer (1990), provides interesting information concerning USDA’s biological control 
programs from 1888 to 1951. 


However, in addition to these added references and a general discussion of the ARS CBC programs, 
a number of important events during the last six years (1994-1999) that have affected ARS programs 
are noted in this Epilogue. The National Program Leaders (NPLs) for Biological Control during this 
period were R. I. Carruthers and K. J. Hackett. E. S. Delfosse joined ARS in 1997 as NPL for Weed 
Science. 


Program Successes: The arthropod and weed pests for which complete or substantial economic 
control has been achieved by CBC, or, in the case of recent programs, for which there is ample 
potential for success, are listed in Table 7. The terms "complete" and "substantial" control are those 
traditionally used in regard to CBC programs (DeBach and Rosen 1991), in which "complete 
economic control" indicates that other control measures are rarely if ever required on a sustained 
basis. In this regard, CBC entomologists are fond of noting that these programs appear to be the only 
such examples in which USDA research has in fact resulted in actual long-lasting economic control 
of a pest. Many examples in which "partial" control of a pest has been achieved by means of 
establishment of one or more exotic natural enemies are not listed in the table. Though footnoted in 
the table, it must be stressed that many other organizations besides ARS have been involved in most 
of the programs listed, for which credit is richly deserved but which are not herein specifically 
indicated. Likewise, ARS has played a role in many projects that were led by state, university, and 
other federal agencies. 


Benefits in terms of annual savings have only been estimated for a few of the classical biological 
control importation programs conducted by the USDA-ARS from 1953 to 1993. This is primarily 
because economists have rarely been included in ARS research programs, and most entomologists 
have little expertise or time to conduct benefit:cost analyses. As noted in Chapters III and IV, the 
ARS programs for which some benefit:cost figures do exist include successful programs against the 
cereal leaf beetle, alfalfa weevil, Rhodesgrass mealybug, pea aphid, and alfalfa blotch leafminer, for 


145 


which a conservatively estimated combined annual savings totals about $150,000,000, in terms of 
1993 dollars, plus increased crop yields. The few extant examples of estimated benefits from 
biological control of weeds projects from 1944 to the present (common St. Johnswort, alligatorweed, 
tansy ragwort, and puncturevine projects) total at least $30,000,000 annually. The resulting total of 
estimated annual benefits from CBC is therefore well over $180,000,000, eight times the estimated 
$21,500,000 spent on all aspects of biological control by ARS in 1987 (Table 8), and represents a 
total grower savings from CBC during the past decade of more than $2 billion (Hays 1992). The 
highly positive benefit:cost ratio of CBC is clearly demonstrated by comparing these savings with the 
estimated total cost ($20 million) of federal and state research on CBC from 1888 to 1976, and the 
estimated $420 million spent annually on insecticides in the 1960s (see Chapter III, and Sailer 1973, 
1976b). (Use of pesticides in the United States in 1995 was estimated to be 1.2 billion pounds valued 
at over $10 billion [Benbroke et al. 1996].) It must be emphasized that most of these estimated 
figures are savings resulting from cessation of pesticide treatments no longer required because of 
permanent biological control of the pests, and do not include the additional (and incalculable) 
environmental benefits. 


Costs of the alfalfa weevil and alligatorweed programs are estimated to have been $1 million each 
(Chapter III). The relatively small costs of CBC result in the highly favorable and often cited 30:1 
benefit:cost ratio for CBC (DeBach and Rosen 1991); the benefit:cost ratio of the alfalfa weevil 
program alone is estimated at 87:1 (Kingsley et al. 1993). CBC is often unfairly criticized for being 
too slow a method of pest control; it often takes five to ten years before populations of introduced 
natural enemies increase sufficiently for adequate control to be realized, although spectacular control 
is sometimes achieved much earlier. However, both costs and control time for CBC compare quite 
favorably with research on pesticide development. It has been estimated that it takes six to 13 years 
and $30-50 million to develop a pesticide from its discovery to registration and marketing (Weil 
1988; Menn and Christy 1992; Hutchins and Gehring 1993). 


Successful augmentative biological control programs have also resulted from CBC research. The 
identification and introduction of the exotic natural enemies Pediobius foveolatus and Edovum 
puttleri were accomplished during CBC explorations. These parasites were found to be incapable of 
establishment in the U.S., but have been successfully utilized in augmentative programs against 
Mexican bean beetle and Colorado potato beetle, respectively (see Chapter IV, section B.1.b). 


In addition to the many positive ARS CBC programs and trends over the past 110 years documented 
in the previous chapters of this history, this history has also documented several negative trends, one 
of which included a sharp decline in the number of scientists, facilities, and programs of the ARS 
biological control effort during the two decades prior to the original drafting of this Epilogue (1993). 
By 1999, however, this trend had reversed dramatically. 


Personnel: Table 8 lists the number of ARS scientists at the end of December 1993 that devoted at 
least half time to CBC of arthropods and weeds, i.e., scientists exploring for, or working on the 
release, establishment and evaluation of exotic natural enemies. Six of the 28 SYs in 1993 were 
devoted to use of pathogens in CBC, an increase from zero in 1972. Five of the other SYs are foreign 
nationals stationed at ARS overseas stations in Europe and South America. Data obtained from the 
ARS Research Management Information System (RMIS) in December 1993 of CBC projects in ARS 
report a total of 31.7 SYs devoted to CBC. This included 13.7 SYs to weed control, and 16.3 SYs to 
arthropod control, and 1.7 SYs devoted to control of plant pathogens. The resulting total of 28 SYs in 
Table 8 is in agreement with the 30 CBC SYs from the RMIS report (excluding the 1.7 SYs for plant 
pathogens), when the RMIS figure is adjusted for loss of two CBC positions late in 1993. 


Tables 9 and 10 show the estimated resources and SYs devoted to each biological control approach 
and research area (including taxonomic research related to biological control) by ARS in May 1987. . 


146 


A total of an estimated 43.4 SYs are listed for CBC. The estimates are considered to be inflated due 
to the survey method in which as little as 10% of a scientist's time devoted to biological control was 
included in the tabulation, thus not presenting an accurate picture of the number of full-time ARS 
scientists devoted to biological control research. Because of this, comparisons among years are not 
entirely valid. 


However, the total of 28 active SYs noted in Table 8 represented a significant reduction from the 43 
SYs reported in 1972 (Sailer 1973; see Chapter III), and from those 1987 figures (Table 10). 


Although the decline in number of biological control scientists within ARS caused some detrimental 
impacts to the success of the program, it represented not a specific reduction to the area of biological 
control research but a more widespread decline of available resources for many different types of 
agricultural research. This general decline was brought to the attention of USDA administrators by 
the current (1999) ARS Administrator, Dr. Floyd P. Horn. Dr. Horn documented that the number of 
ARS scientists has declined from an all time high of approximately 3,400 in the early 1970s to a low 
of 1,685 in the mid-1990s. This was over a 50% reduction in the number of scientists of all 
categories employed by ARS over an approximate 20 year period. Dr. Horn has made it an Agency- 
wide priority to reverse the downward trend and to again bolster the number of ARS scientists 
working on all types of agricultural research. 


At the end of fiscal year 1999, ARS had expanded those numbers to over 1,900 Category 1 Research 
Scientists and had targeted a goal of 2,000 active Category | Scientists by the beginning of calendar 
year 2000. In working to accomplish this goal, biological control has been one of the disciplines that 
benefitted. 


In 1999, records from 49 ARS locations where some biological control work was reported indicated a 
total of 188.4 SYs in all aspects of biological control research: 35.9 in CBC, 10 in conservation 
biological control, 38.9 in augmentation, 44 in microbial control, and an additional 59.6 conducting 
unspecified type of biological control research. Further, these SY figures can be considered to under 
represent ARS effort because foreign service nationals working at ARS overseas laboratories on 
CBC are not included in the tabulation. The total ARS biological control budget was reported to be 
$64,850,800: $12.5 million in CBC, $3.2 million in conservation, $14.0 million in augmentation, 
$16.1 million in microbial biological control, and the remaining $19.1 million in unspecified types of 
biological control. 


Based on the leadership of Dr. Horn, additional new funds and over 20 new scientists were added to 
the ARS biological control program in several locations and included expansions primarily for 
classical and augmentation biological control. During this period, new positions were added: to 
Stoneville, MS, to address the biological control of tropical soda apple, termites, and general 
research on augmentation biological control diet development and engineering (4 positons); to 
Weslaco, TX, for augmentation biological control and insect pathology (2 positions); to Orlando (Ft. 
Pierce), FL, for biological control of vegetable and horticultural pests (2 positions); to Gainesville, 
FL, for natural enemy diet development (1 position); to Ft. Lauderdale, FL, for biological control of 
melaleuca (2 positions); to Newark, DE, for biological control of Asian longhorned beetle (1 
position); to Beltsville, MD, for biological control of Colorado potato beetle and gypsy moth (2 
positions plus additional technical support for the BCDC); to Ames, IA, for insect pathology and 
assessment of Bt resistance management (1 position); to Albany, CA, to enhance classical biological 
control of weeds, particularly yellow starthistle (2 positions plus additional resources for the 
quarantine operation); to Sidney, MT, for biological control and IPM of grasshoppers (2 positions); 
to Columbia, MO, for biological control of weeds and augmentation biological control diets (1 
position); and to Montpellier, France, for the addition of a plant pathologist to study classical 
biological control of weeds (1 position). In addition, ARS has further partnered with USDA-APHIS 


147 


at several locations to enhance joint biological control activities and through this program has added 
a new position to the Albany biological control of weeds facility (quarantine officer and weed 
biological control scientist) in a new joint program. 


While the general trend was therefore positive, some areas, e.g., systematics research, did not fare as 
well. There had been a severe loss of expertise in insect taxonomy in ARS, an area of research that is 
critical to biological control as noted by many authors (e.g., Sabrosky 1955; Knutson 1981). Since 
1972, the number of research scientists in the ARS Systematic Entomology Laboratory (SEL) has 
fallen from a high of 32 (in 1972) to a total of 22 (and 18 in 1999) (M. B. Stoetzel, SEL, personal 
communication, 1993, [1999]). This included the loss of taxonomic expertise in the hymenopterous 
families Ichneumonidae (position lost in 1980) and Braconidae (position lost in 1993), families that 
contain the wasp parasites extensively used for biological control of arthropod pests. Taxonomic 
expertise in other families of importance to biological control (e.g., weeds, nematodes, microbial 
organisms) was also inadequate in ARS to meet current biological control research needs. 


- In the late 1990's, ARS did provide a new molecular systematics position to the Systematic 
Entomology Laboratory (1 position) and established a headquarters fund to assist in systematics 
issues linked to exotic pests and biological control (currently funding efforts on Asian longhorned 
beetle). Additional support for systematics was recognized as needed. 


Facilities and Programs: Beginning with the loss of the West Coast Parasite Receiving Station at 
Riverside, CA, in 1968 (see Chapter III), CBC research at a number of other ARS facilities had been 
terminated or phased down by 1993. As indicated below, this trend was mostly reversed by 1999. 


The Research Quarantine Facility at Stoneville, MS, planned by the Insect Identification and Parasite 
Introduction Research Branch (IIPI) prior to the 1972 ARS reorganization as a southeastern regional 
quarantine facility for receipt of exotic natural enemies for both arthropod pests and weeds, 
functioned as such until the mid-1980s (Jones et al. 1985). But until recently it was severely under- 
utilized with little or no CBC research at that location. A new Augmentation Biological Control 
Facility has now been designed and funded for construction in Stoneville, MS (construction 
scheduled for FY 2000). The Stoneville quarantine facility has also been brought back on-line, and 
quarantine studies for tropical soda apple have been initiated. 


The CBC entomologist at Columbia, MO, who operated a small quarantine facility there, was not 
replaced after his retirement in 1989, leaving no ARS CBC research or ARS quarantine capability in 
the north central states. A scientist has recently been added there to conduct research on 
augmentation and biological control of weeds. CBC research at the ARS Plant Science and Water 
Conservation Laboratory at Stillwater, OK, involved in the Russian wheat aphid program, has also 
not been replaced following a retirement in 1993. 


In 1996, the scientists conducting CBC research on weeds at the ARS Rangeland Weeds Laboratory 
in cooperation with Montana State University personnel and the quarantine facility at Bozeman were 
moved to Sidney, MT, where a small new quarantine facility is (1999) in the planning stage, and 
where several new biological control scientists have been hired following a local redirection of 
program activities. 


The staff of the quarantine facility at Newark, DE, the primary ARS quarantine for exotic parasites 


and predators, was cut from five to three scientists by the end of 1993; but as noted above, the 
positions have been restored. 


The staff of the quarantine facility at Albany, CA, once the primary ARS quarantine for exotic 
invertebrate natural enemies of weeds, was reduced from five SYs to one by 1993 (see Chapter IV, 


148 


section C; Goeden 1993). However, some of the recent additional funds have resulted in 
establishment of a new biological control program, the “Exotic and Invasive Weed Research Unit” at 
the Western Regional Research Center at Albany. This consolidated Research Unit includes the 
biological control of weeds personnel and quarantine facility at Albany, the rangeland weed program 
at Reno, NV, and the aquatic weed control unit at Davis. And the Albany quarantine facility has been 
significantly up-graded since 1997. 


The former "Biological Control of Insects Laboratory" at Tucson, AZ, at which some CBC research 
was conducted, though research there was primarily related to augmentation, became the "Honey Bee 
Research Unit" as of 1993; biological control research there was transferred to the Western Cotton 
Research Laboratory at Phoenix. 


Personnel of the former "Beneficial Insect Introduction Laboratory" (BIIL) at Beltsville, MD, were 
placed in 1990 in Beltsville's "Insect Biocontrol Laboratory," which consisted mainly of insect 
pathology research; the former northeastern biological control of weeds program of BIIL was 
terminated in 1993 (see Chapter IV). 


By 1999, one of the two CBC scientists at the ARS quarantine facility at Temple, TX, had retired, 
leaving that facility in danger of termination upon the retirement of the second scientist. 


By 1993, staffs of the ARS overseas biological control laboratories in Europe (EBCL) and South 
America (SABCL) had been trimmed; the new ARS facility in Australia (ABCL) was being 
supported only with "soft" funds (i.e., by non-ARS funds, in this case by temporary funds from a 
coalition of two other federal [U.S. Army Corps of Engineers and National Park Service] and six 
Florida state and county agencies); and the former Asian Parasite Laboratory in South Korea was 
closed in December 1993, despite the recent introductions of Asian pests (e.g., the "Asian" gypsy 
moth, brown citrus aphid, Asian longhorned beetle) (see Chapter IV). Program support by ARS for 
the cooperative Sino-American Biological Control Laboratory in Beijing, China, has recently been 
strengthened to help meet this need. By 1998, base ARS funds had been added to the Australian lab 
to support the SY there. It can also now be noted that the newly constructed facilities of the European 
Biological Control Laboratory at Montpellier, France, were completed and occupied in October 
1999, and that a plant pathologist had been added to the staff there for biological control of weeds. 
And by 1999, ARS funding of the South American Biological Control Laboratory had been 
stabilized. 


Some other reasons for the temporary decline in CBC research in ARS were noted in a paper entitled 
"Classical Biological Control: An Endangered Species" by J. J. Drea (1993), an ARS CBC retiree. 
Because of its nature, CBC research generally cannot be easily commercialized and thus is usually 
supported by public funds, both federal and state, rather than by private industry. Drea noted that 
there had been some conversion of positions to biotechnology (genetic engineering and molecular 
biology research, which require extremely expensive equipment and supplies and extensive support 
personnel; see also Freistadt 1988). Funding of CBC is also negatively affected by an expectation of 
instant gratification (CBC alone is not a suitable pest control tactic in all cases, but neither is any 
other single control method) and the long budget cycle (which, by long-term allocation of funds for 
specific purposes, limits flexibility to meet changing conditions and new target pests), as well as 
personnel in leadership positions. Many of these points have recently been addressed by ARS 
administrators, and benefits of CBC have again been realized and the negative trend in funding 
reversed. 


Although the temporary shifts of personnel and programs to other disciplines reported above caused 


ARS CBC to decline for a number of years, the importance of the USDA CBC program and the 
demand expressed by stakeholders benefitting from the program caused an upsurge in ARS funding 


149 


and many new positions since 1993, as noted above. Not only have base-funded programs been 
increased, but ARS has now devoted several million dollars to an Area-wide IPM program for 
control of leafy spurge using CBC as the central control technology, and has taken steps to meet the 
influx of several new invasive weed and arthropod species, such as tropical soda apple, the Asian 
longhorned beetle, and pink hibiscus mealybug. 


Program coordination: One important area not mentioned by Drea (1993) that seriously affects CBC 
in the United States is the lack of coordination of CBC research and implementation programs at all 
levels. As indicated in Chapter IV, sections A, B.1.a, and C, program coordination within the ARS 
was a serious problem by the end of 1993. The 1971-72 reorganizations of ARS destroyed the 
effective coordination of previous years, when CBC research in ARS, from overseas exploration and 
study, through quarantine research and clearance, to field release and evaluation, was administered 
and coordinated by a single ARS office. A similar loss of centralized direction of USDA's CBC 
activities occurred at the establishment of ARS in 1953, but was soon thereafter reestablished (except 
in regard to forest pests); see Chapters III and V. Frequent reorganizations within the USDA and 
ARS described in the above chapters certainly were of little help with regard to CBC in the U.S. 


In addition, since 1972, nearly all ARS laboratories have ceased producing detailed periodic reports 
on their research, greatly reducing communication and coordination. 


Attempts to reestablish effective coordination of ARS CBC research since 1972 to 1993 have 
included establishment of various Working Groups, Coordinating Subgroups, Technical Advisors, a 
"National Biological Control Program," and a "Biological Control Matrix Team" within the ARS 
National Program Staff (NPS), but problems still existed; see Chapter IV and Appendix I.A. A major 
difficulty has been that responsibilities for coordination of classical biological control research 
within ARS are severely diluted. Major coordination responsibility until recently was placed largely 
in the hands of one National Program Leader (NPL) for Biological Control in the NPS, whose 
responsibilities since 1993 include not only biological control and insect taxonomy, but also other 
pest management systems; recently CBC of weeds research projects were moved under the direction 
of the new NPL for Weed Science. On the other hand, all of ARS's overseas laboratories, including 
those conducting biological control research, were administered by the Office of International 
Research Programs (OIRP) (by 1999, administrative responsibility for a few of them were placed 
elsewhere); and within the NPS, other NPLs are responsible for coordination of ARS research on 
weeds, applied, and medical and veterinary entomology, and other related research areas that include 
biological control, but goals of which are often in competition with, or conflict with, those of CBC. It 
must be stressed that responsibilities of the position of NPL for Biological Control (no longer labeled 
“for Pest Management Systems”, but includes insect taxonomy), are carried by a single staff scientist 
whose many duties require his time to be spread extremely thin, who has no full time technical 
assistance, and who may or may not have a broad background in biological control. Much the same 
responsibilities, but related specifically to biological control and taxonomy, were borne by three 
biological control/taxonomy specialists, each with technical and clerical staff, who administered the 
Insect Identification and Parasite Introduction Research Branch (IIPI) of ARS prior to the 1972 
reorganization. Other current problems are many and include the fact that the NPS Biological Control 
Matrix Team did not function as an effective coordinating body (and was abolished), nor do the 
Biocontrol Working Groups function, as intended, as effective advisory bodies for the NPL. A 
fundamental problem is the quantity of paperwork and growing interagency coordinating 
responsibilities that hamper legitimate research coordination activities on the part of the NPLs. 


Ideally, an effective CBC program needs to be centrally administered, with consequent avoidance of 
divided responsibilities among organizations for the various sequential activities involved. This has 
been pointed out by several authors (e.g., Beirne 1985; Sailer 1974, 1976b, 1981b). The three cited 
articles by R. I. Sailer, the last administrator of such a coordinated program in ARS, describe an 


150 


idealized program in detail. One major benefit of such a centralized organization (as existed prior to 
1972) was the ability to move funds, other resources, and personnel quickly in response to 
emergencies and other program considerations. This included rotation of personnel from overseas to 
domestic locations and vice versa, and a close tie between the overseas laboratories and domestic 
program needs. 


Coordination of CBC programs on a larger scale, i.e., USDA-wide and within the United States, is 
also badly needed (for weeds, see Goeden 1993). Broader coordination of CBC by the IIPI prior to 
1972 was aided by Memoranda of Agreements between various other federal, state and university 
organizations, and the Special Foreign Currency (SFC, or PL480) program, and detailed reporting 
requirements; see Chapter III and Chapter IV, section B.1.a, and Appendix I.C. The development of 
CBC activities in other USDA agencies since 1980, particularly the Animal and Plant Health 
Inspection Service and Forest Service, requires better coordination than now exists. Attempts have 
been made to provide such coordination since 1972 by establishment of a Working Group on 
Biological Control Agents (WGBCA) and later by the Interagency Biological Control Coordinating 
Committee (IBC*); see Chapter IV, section A, and Appendix I.B; these attempts were only partially 
successful. 


As federal research on CBC diminished in the past 25 years, there has been a corresponding increase 
in CBC research and implementation at U.S. universities, with an increase in the number of 
biological control quarantine facilities, all of which has increased difficulties in providing overall 
coordination of CBC within the U.S. To assist in this regard, representatives of the Cooperative State 
Research Service (CSRS) and Extension Service, USDA's agencies administering federal funds for, 
and coordinating research and extension activities at State Agricultural Experiment Stations (SAES) 
at U.S. land-grant universities, were added to the WGBCA and IBC’, but effective coordination 
between federal and SAES CBC research and implementation at the national level remains a 
problem; some regional coordination is effected by means of CSRS-sponsored Regional Research 
Projects, which include SAES and ARS scientists. CSRS and Extension Service were combined in 
1993 as the Cooperative State Research, Education, and Extension Service (CSREES). 


Also, the reduced federal CBC program has negatively impacted biological control implementation 
programs of some State Departments of Agriculture; representation of the interests of such state 
programs was added to the IBC’ by means of liaison representation of the National Association of 
State Departments of Agriculture (NASDA), but coordination attempts were minimal. 


Problems between state, federal and university scientists have existed almost from the beginning of 
CBC in the United States; see Chapter I. Conflicts arise over competition for funds, initiatives for 
basic versus applied research, and often the lack of formal training in CBC by ARS and other federal 
scientists involved in CBC research programs; the development of CBC implementation activities in 
APHIS and the states has complicated the situation (Goeden 1993). To meet those conflicting 
concerns, more funding for all aspects of CBC (including taxonomy) is required, more basic and 
theoretical research is needed (to help resolve some of the perceived problems in CBC [e.g., see 
Beirne 1985]), but not at the expense of applied research leading to control of serious introduced 
pests, and more highly trained CBC scientists are needed in the federal programs. Also, there are 
strong objections on the part of a few SAES scientists to perceived attempts to control (i.e., 
coordinate) biological control in the United States by ARS, or APHIS; coordination is needed at a 
higher level in USDA than from either agency. These current competitive attitudes among CBC 
scientists, whether in federal, state, and university programs, hamper good communication among 
workers and coordination of CBC throughout the country, and seem to require effective high level 
coordination to alleviate. A stronger relationship between all three areas, but particularly between 
USDA and SAES scientists, than exists today is needed. There has been recent improvement in this 
area through the CSREES Regional Projects, which involve both SAES and USDA scientists. 


151 


Coordination of a national biological control program has not yet been demonstrated, and a national 
policy in this regard is long overdue. Numerous recommendations to provide mechanisms for such 
coordination, within the USDA, have been proposed; see Chapter IV, and Ehler (1991), ESCOP 
[1989], and the many related recommendations made by the scientific community at a number of 
biological control conferences and workshops during the past 15 years (USDA 1978, 1984a; 
Battenfield 1983; King et al. 1988; Coulson et al. 1991). These many carefully considered 
recommendations, most made at great expense by groups of biological control scientists, have 
unfortunately been ignored. 


Coordination efforts such as the IBC’ could have conceivably been reorganized, with strong 
involvement of the SAES and all appropriate USDA agencies, to establish a "permanent biological 
control committee to coordinate a ‘National Biological Control Program'". Such a structure was 
proposed by the Experiment Station Committee on Organization and Policy (ESCOP), Working 
Group on Biological Control (ESCOP [1989]; Ehler 1991a). The establishment of a national planning 
body for biological control was in fact proposed much earlier in a report by the Office of Technology 
Asssessment (OTA 1979); see Chapter IV, section B.1.a. A similar proposal, for different reasons, 
for establishment of a "Division of Biological Control" within USDA (or EPA) has been made 
(Miller and Aplet 1993); see sections on regulations and databases below. More recently, a 
"Directorate for Biological Control" (presumably within USDA) was proposed, under which a 
"National Biological Control Program", as proposed by the IBC* and ESCOP's Working Group on 
Biological Control, would be conducted (Cate and Hinkle 1993). 


Since 1993, there has been some improvement in regard to coordination of CBC within the USDA. 
At the request of Richard Rominger, Deputy Secretary of Agriculture, the NPS (Drs. Carruthers and 
Delfosse) arranged for an “Invitational Workshop on USDA Activities in Biological Control”, which 
was held in October 1996 in Riverdale, MD. This workshop brought together about 80 individuals 
from four USDA agencies (APHIS, ARS, CSREES and FS) and representatives from the EPA, State 
Departments of Agriculture, and Land Grant Universities to discuss biological control coordination, 
regulation and accountability. As far as coordination is concerned, this workshop resulted in the 
establishment of a USDA Biological Control Coordinating Council (BCCC) with the responsibility 
of developing an action plan to implement the Workshop’s recommendations. The BCCC is 
composed of senior executive managers of APHIS, ARS, CSREES and FS with oversight 
responsibilities for biological control programs, biological control policy, and allocation of program 
resources within their respective agencies. Also established was an Inter-Agency Advisory and 
Action Team (IAAT) to serve as the operational arm of the BCCC to facilitate all elements of 
USDA’s biological control programs. See Carruthers and Petroff (1997) and Carruthers and Delfosse 
(1998) for more information. It remains to be seen how effective the BCCC and IAAT will be in 
providing effective coordination of CBC on a national basis. 


But coordination of a national program is not enough. There is also a need for international, 
particularly North American, coordination in biological control. Reestablishment of the 
communication and coordination between U.S. and Canadian biological control programs that 
existed prior to the 1972 reorganization of ARS is needed. Prior to the reorganization, annual 
meetings between IIPI and Canadian forestry and agricultural biological control administrators were 
arranged to discuss and coordinate the CBC programs of the two countries. Efforts to continue such 
coordination after the reorganization were largely unsuccessful. Some coordination of Canadian and 
U.S. exploration programs in Europe has been accomplished by annual meetings there involving not 
only ARS and Canadian programs carried out by the International Institute of Biological Control 
(IIBC), but also Australian program interests in Europe. The North American Plant Protection 
Organization (NAPPO), established in 1976, attempts to exchange information and provide some 
coordination of plant protection activities of Canada, the U.S., and Mexico. Country representatives 
on NAPPO are from Agriculture Canada's Plant Health Division, USDA's APHIS, and Mexico's 


152 


Direccion General de Sanidad y Proteccién Agropecuaria y Forestal. A Biological Control Panel 
exists within NAPPO, but there is no formal representation from ARS or other research 
organizations. Coordination of CBC activities with the developing programs in Mexico is becoming 
increasingly important. The lack of close coordination of such programs between the U.S. and 
Canada has been most troublesome in regard to biological control of weeds programs; see Chapter 
IV, section B, and below. Coordination of U.S. CBC programs on a broader international scale, 
involving potential cooperative programs of the IIBC, Australia, and various South and Central 
American, European, African, and Asian countries, is also highly desirable. Such international 
coordinative and cooperative activities in CBC does not seem to fit well in the role of the BCCC as 
presently organized. 


Special Problems in ARS Classical Biological Control of Weeds Programs: The cost of a biological 
control program for a weed using foreign control agents, or of a testing program to clear one such 
agent for release in the U.S., is generally far greater than for a similar program to control an 
arthropod pest. This is because of the additional research necessitated by the generally acknowledged 
danger of attack by the introduced control agent on non-target plants, particularly beneficial plants 
that could include major crops. There has been increasing concern in this area in the CBC of 
invertebrate pests. 


These problems are well understood and research protocols have been developed over the years that 
have produced excellent control of many weeds and have never resulted in significant, long-term 
damage to any beneficial plants. Since promulgation of the Endangered Species Act in 1973, 
concerns over endangered and threatened native plants has increased in ARS programs. 


The incipient dangers involved in biological control of weeds demand extreme care in conducting 
host-specificity testing both overseas and in domestic quarantine, requiring three to five years before 
field releases are made. A large amount of time is spent 1) in the planning stage of a project 
(particularly in selection of appropriate target weeds and resolution of conflicts of interest between 
beneficial and harmful qualities of the weed), 2) in careful, long-term, coordinated explorations for 
natural enemies and selection of the best agent among many to test, 3) in the testing process itself 
(including both safety and efficacy testing) and in developing quarantine culture techniques, and 4) 
in obtaining approvals for field release, before the agent can be field released, and long before any 
results of the research can be demonstrated by any degree of weed control. 


Fragmentation of the lines of communication under the present ARS organizational structure has 
often impeded progress in biological control of weeds programs, resulting in some delays in initiation 
and completion of programs, poor coordination between U.S., Canadian, and overseas researchers 
and state and federal (APHIS) "implementers" (Goeden 1993), and missed or delayed opportunities 
for successful projects. Although the NPS was established for program coordination, it has not in the 
past fully met the needs in regard to CBC of weeds, which had involved two NPLs -- one with 
responsibility for research on weed control and one with responsibility for research on biological 
control of pests, including weeds. Reasons, as discussed above and in previous chapters, include the 
often short duration that pertinent NPLs occupy their positions in NPS, significant periods during 
which one or the other NPL position is unoccupied, lack of in-depth knowledge peculiar to biological 
control of weeds by the incumbent NPL, and demands on the time of the NPLs to provide budgetary 
and other information to higher administrative levels which leaves little of their time for program 
planning and coordination with scientists in the field. Since 1993, there has been major improvement 
in this area. In particular, biological control of weeds has been placed under jurisdiction of the NPL 
for Weed Science. However, weed science encompasses a large area, and depending on the person 
occupying that NPL position, biological control of weeds could again be de-emphasized in the future. 


153 


One other problem that affects primarily weed programs is that a number of weed targets amenable to 
CBC are not "agricultural" problems, e.g., the several aquatic weeds that have been targeted, as well 
as the wetland weeds melaleuca, saltcedar, and purple loosestrife. As noted in previous chapters, in 
order for ARS researchers to address problems with such weeds, "soft" money, i.e., funds from other 
agencies, has generally been required, rather than regular ARS funds. This has caused some 
continuity problems in some of the research programs affected. One of the reasons for the 
termination of the ARS purple loosestrife program was the fact that the weed was not an 
"agricultural" weed; funding for the Australian laboratory, which provides ARS overseas research on 
melaleuca natural enemies, has also been in jeopardy. Recent public concerns over “invasive 
species”, expressed first in the 1993 OTA report on non-indigenous species (OTA 1993), and more 
recently President Clinton’s 1999 Executive Order on Invasive Species, has lessened the extent of 
this problem in ARS, though the Forest Service has begun to play a larger role in this area. 


Regulations: Another development during the past 25 years that has had an impact on CBC in the 
United States is the gradually increasing strictness of safety evaluations and procedures inherent in 
the research process leading to the importation and release of exotic biological control agents, in 
response to scientific and societal environmental concerns (Coulson and Soper 1989; Lima 1990). A 
study by the congressional Office of Technology Assessment (OTA) identified CBC as one of a 
number of pathways for the introduction of harmful non-indigenous species (NIS) in the U.S., and 
noted that current regulations regarding the importation of all NIS were inadequate (OTA 1993). 
Some specific problems adding to environmental concerns directed at CBC include: perceived 
environmental damage caused by CBC in the past (e.g., see Howarth 1991; Miller and Aplet 1993); 
controversy over the use of exotic agents to control native pest organisms (e.g., see DeLoach 1978, 
1995; Andres 1981; Hokkanen and Pimentel 1984; Goeden and Kok 1986; Ehler 1991b; Lockwood 
1993 a and b, Carruthers and Onsager 1993); the potential hazard of overseas collections and 
introductions of exotic "biological control agents" by amateurs or non-specialists (Coulson and Soper 
1989); and the recent increase in commercial shipments to the U.S. of biological control agents from 
foreign commercial suppliers, and shipments within the U.S. of many domestic and foreign natural 
enemy species by domestic commercial concerns (e.g., see OTA 1993; Frank and McCoy 1994). 


The CBC scientific community has attempted to provide technical input for the use of regulatory 
agencies in considering development of specific regulations for CBC to address the environmental 
concerns (Coulson et al. 1991; Charudattan and Browning 1992; FAO 1992). There is concern 
among CBC scientists that regulations to be developed may become so strict that CBC research in the 
U.S., which has admirable success and safety records to date, could be brought to a near halt, and 
some aspects of recently published proposals have increased this concern (Howarth 1991; Miller and 
Aplet 1993). This concern would appear to be a real possibility, unless funding of CBC research 
were increased significantly to meet strict requirements for considerably more detailed pre- and post- 
introduction safety and environmental studies. For example, Miller and Aplet (1993) proposed that 
each biological control agent be subjected to public review as to potential effects on all "native 
organisms" in each new U.S. ecosystem into which the agent is proposed for release, "as well as 
[those in] neighboring ecosystems likely to be invaded [by the agent]." They also recommend 
passage of a U.S. Biological Control Act, establishing a Biological Control Division within the 
USDA (or EPA) with "authority to issue regulations governing the collection of required information 
about each biocontrol application, review all proposals, and ensure that follow-up studies assess the 
actual impact of biocontrols on both target and non-target organisms and on the ecosystem as a 
whole." 


The OTA report on harmful non-indigenous species (NIS) (OTA, 1993) also made several 
recommendations pertinent to this discussion. Noting that the U.S. had suffered a loss of over $92 
billion from only 43 of the many introduced insects from 1906-91, the report noted a need for a "real 
national policy" on harmful introductions and continued research and development on ways to 


154 


manage harmful NIS. Other needs mentioned were "solid databases (with information from foreign 
sources) and substantial taxonomic expertise," noting that "accurate and timely species identification 
is essential but sometimes not available." (In regard to CBC, such taxonomic expertise is needed for 
both pest and natural enemy taxa; see comments below regarding databases.) The OTA report went 
on to recommend "careful post-release monitoring" of planned releases (e.g., of biological control 
agents), i.e., follow up impact studies. These kinds of studies, which many scientists agree are highly 
desirable, will require significant additional funds for CBC research. (In fact, it is now [1999] ARS 
policy that all CBC for weeds program proposals must include provisions for follow up impact 
studies in order to be funded.) 


Finalization of ARS guidelines and procedures for introduction and release of non-indigenous 
biological control agents has been held in abeyance pending finalization of pertinent procedural 
guidelines and regulations by APHIS (Coulson et al. 1991). No such proposed regulations or 
guidelines were published by APHIS by the end of 1993, leaving many scientists in a quandry as to 
standard procedures to be followed to obtain official clearance for field release of introduced 
biological control agents. 


In 1999, problems still existed in this area. In 1996, APHIS published a Proposed Rule with the 
determination that natural enemies of invertebrates were not plant pests and thus were no longer to be 
regulated by APHIS (Carruthers and Petroff 1997). The regulation of natural enemies of weeds was 
still to be a responsibility of APHIS. Some of the increased ARS funds for biological control resulted 
in the establishment of a new position in the ARS Biological Control Documentation Center (BCDC) 
to serve as a liaison position to aid ARS scientists in meeting legal requirements for classical 
biological control introductions and other areas. The position was also charged with development of 
ARS biological control procedures to meet all legal requirements for classical and other types of 
biological control research, which became a priority necessity after the 1996 APHIS decision. 


As of November, 1999, passages in the proposed consolidated statutes in the U.S. Congress can be 
interpreted to include placement of entomophagous agents under the jurisdiction of APHIS. This 
issue is likely to be an evolving one. 


Databases: There are a number of technical databases developed by ARS that are of importance to 
classical and other types of biological control, and also to the "National Partnership for Biological 
Survey" of the nation's biological resources proposed by the U.S. Department of Interior (ESA 1993), 
and to the question of introductions of non-indigenous species (NIS) into the U.S. In February 1999, 
President Clinton signed an Executive Order on Invasive Species. One of the needs identified was for 
coordination of information on this subject, both nationally and internationally. In this regard, a 
Workshop on Invasive Species Databases was held in Las Vegas in November 1998, the Proceedings 
of which has been published (Ridgway et al. 1999). Some of the pertinent ARS databases were 
among those summarized in that document. These included several Systematic Entomology 
Laboratory databases on arthropods, the U.S. National Fungus Collections Database of the 
Systematic Botany and Mycology Laboratory, and the "Releases of Beneficial Organisms in the 
United States and Territories" (ROBO) database (Coulson 1992b). Not included in the 1999 
publication were databases of ARS’ Nematology Laboratory’s USDA Nematology Collection and the 
Entomopathogenic Fungal Culture database (Humber 1992). All these databases are now (1999) 
available via the Internet. Lichtenfels et al. (1998) provide updated information on ARS systematic 
collections and databases. Because of limited resources, these and other databases have unfortunately 
received low priority among many agricultural research needs to be addressed by ARS. 


ARS also developed the "North American Immigrant Arthropod Database" (NAIAD) (Knutson et al. 


1990), but this was never adequately funded. Consequently, this database formed the basis of the 
“North American Nonindigenous Arthropod Database (NANIAD) developed by Pennsylvania State 


Ne) 


University, listed in Ridgway et al. (1999). ROBO records the importation and release of non- 
indigenous beneficial invertebrate and microbial organisms into the U.S., whereas NANIAD records 
the establishment in the U.S. of non-indigenous arthropods, harmful, beneficial, or otherwise benign. 
Both databases meet the need stated in the OTA report (OTA 1993) to include extensive "information 
from foreign sources" regarding NIS, particularly NANIAD. ROBO currently resides in the ARS 
Biological Control Documentation Center (BCDC) together with extensive biological control files 
and a library; BCDC thus serves as an information source for biological control, one suggested 
function of the so-called "Division of Biological Control" recommended by Miller and Aplet (1993). 
ROBO, which was made available on the Internet in 1999, contains nearly 20,000 records of 
importations and releases of exotic biological control agents and pollinators from 1981 through 1985. 
A second position was added to the ARS Biological Control Documentation Center in 1999, which 
will aid in updating the database. 


The Future for Federal Classical Biological Control Programs: The sections dealing with CBC of 
arthropods and weeds in previous chapters of this history, and earlier comments in this Epilogue, 
have indicated the benefits of a federal CBC program. They have also indicated a number of 
problems and drawbacks of the program, many of which have been addressed in recent years. It can 
be demonstrated that there is a compelling need for the continuation and augmentation of a strong, 
well-coordinated federal CBC program. 


Introductions of harmful non-indigenous organisms into the U.S. will certainly continue and are 
expected to increase in number. This is due to increased international trade and tourism, the increase 
in containerized shipments of goods, and a possible change in APHIS pest exclusion policies leading 
toward elimination of "plant pest regulations as trade barriers". The latter may result in lessened 
detection and other actions designed to prevent plant pests from entering the U.S., which is perceived 
as eventually "an unrealistic goal" (OTA 1993; APHIS, PPQ 1993); although the 1999 Executive 
Order on Invasive Species may increase detection efforts. It can be expected that the numbers of 
potential targets for classical biological control are very likely to increase significantly. The list of 
exotic weeds in the U.S. that can be targeted for CBC research is already long and is growing (USDA 
1984a; DeLoach 1991a; OTA 1993). 


Some states, such as California, Hawaii, and Florida, have experienced an influx of an unusually high 
number of exotic pests specific to their particular ecosystems, climate, and agricultural and cultural 
history (Frank and McCoy 1992; OTA 1993). Because of this, these states have had a strong interest 
in, and have developed, CBC programs tailored to meet their specific needs. These programs have 
been highly successful (Clausen 1978; DeBach and Rosen 1991; Funasaki et al. 1988; Frank and 
McCoy 1993; Rosen et al. 1994) and have truly met the needs of those states. USDA CBC programs, 
on the other hand, have generally dealt with introduced pest problems that are of broader (regional or 
national) scope. It seems quite worthwhile to continue this "division of labor," although better 
coordination and communication between federal and state programs is highly desirable. However, a 
proliferation of probably under-utilized state quarantine facilities in each of the 50 states is certainly 
unnecessary, and would compound the problem of coordination and increase the hazard of unwise 
quarantine actions. Several CSREES Regional Research Projects have been designed to provide 
communication, but have not been particularly effective in providing coordination of national 
programs involving many agencies and people in many states in several regions. 


For these several reasons, there is need for a strong nationally focused biological control policy, to 
include: 1) strengthened, well-coordinated and funded federal CBC research and implementation 
programs, in close partnership with state government and university biological control programs; 2) 
increased support for pertinent taxonomic research and identification services at both federal and 
state levels to support these programs; and 3) a national biological control information center to 
assist in communication and coordination, and to maintain a library and databases of importance to 


156 


classical and other types of biological control. Some suggestions regarding program coordination are 
included in comments in this Epilogue above, including the recent establishment of a Biological 
Control Coordinating Council (BCCC) within the USDA. 


In regard to a strengthened federal CBC program, it has been proposed, in an unfinished and 
unpublished ARS Strategic Plan entitled "Biological Control for the 21st Century", that a federal 
CBC research capability be provided for most if not all major agroecosystems vulnerable to invasions 
by harmful non-indigenous organisms, again in close association with state, university, and other 
federal biological control programs. Needs for regional federal biological control quarantine facilities 
were discussed in a 1991 USDA workshop (Coulson et al. 1991). Such regional capability was absent 
when the cereal leaf beetle was first found in the Midwest in the 1960s (see Sailer 1976b), and is 
severely lacking in the present federal program. Furthermore, it would be well to expand such federal 
biological control capability beyond "agroecosystems" to include CBC targets in urban and "natural 
areas," the latter of which the USDA has been accused of neglecting in regard to effects of harmful 
non-indigenous species (OTA 1993). 


The record of successful control of introduced pests by federal CBC programs representing savings 
of billions of dollars in control costs and immeasurable ecological benefits is noted above. The slow 
decline in the federal research program and its recent improvement has also been discussed above. 
Assuming a continuation of recruitment of trained CBC scientists, the pivotal problem remains a lack 
of a cohesive national CBC policy and coordinated federal research program. Whether current 
departmental coordination efforts, either by the BCCC, the National Biological Control Institute 
(NBCI; see Chapter VI, section C), or another USDA coodinating mechanism not yet in existence, 
can be of any assistance in establishing a real nationally coordinated classical biological control 
program remains to be seen. 





B. SUMMARY OF ACCOMPLISHMENTS OF ARS ON INSECT CONTROL WITH 
MICROBIAL ORGANISMS. By P. V. Vail 


The following pages present a brief summary of the research of the Agricultural Research Service 
reported in more detail in Chapters I-IV above, and particularly in Appendix II below. 


The USDA received early recognition for its research on insect pathology/microbial control. In the 
early 1900s, extensive projects were begun on microbial control of the newly introduced Japanese 
beetle. Also, the impact of pathogens on honey bees was recognized and research began on ways to 
control bee diseases. These early projects emphasized surveys, epidemiology, pathology, and 
descriptions of relevant organisms, and provided important information bases for future basic and 
applied research for solving the problems. As mentioned by Steinhaus (1949), these Japanese beetle 
and honey bee projects provided the stimulus for modern-day programs and the acceptance of insect 
pathology and microbial control as distinct disciplines. 


These developments led to the first extensive use of insect pathogens, “milky” disease organism(s), 
for control of the Japanese beetle. Steinhaus (1949), Clausen (1956), Fleming (1968), and Cameron 
(1973) discussed the importance of this achievement. The organism is still used for control of the 
Japanese beetle. The studies of honey bee diseases are also considered to be classics. Programs on 
both of these problems have expanded to include numerous target species and virtually every type of 
insect pathogen. The establishment of insect pathology as a discipline combined with the foresight of 
E. F. Knipling led to the establishment of insect pathology and microbial control programs at many 
ARS locations throughout the U.S., including the Insect Pathology Pioneering Research Laboratory 
at Beltsville, MD, beginning in the late 1950s. ARS programs developed during the 1960s and 1970s 
had more insect pathology/microbial control specialists than any other institution in the world, and 


157 


conducted diverse research on a variety of agricultural and man and animal pest species and their 
pathogens. 


In the 1950s and 1960s, the adverse effects of a protozoan (Zimmack and Brindley 1957; Lewis et al. 
1971) and a fungus (York 1958) on European corn borer were demonstrated. ARS scientists 
conducted early studies on the potential use of baculoviruses for insect control (Elmore 1961; Elmore 
and Howland 1964). Also in the 1960s research on all aspects of the production, efficacy, and safety 
of a baculovirus led to the first registration of a baculovirus for commercial use (Ignoffo and Couch 
1981). ARS scientists were deeply involved in the development of Bacillus thuringiensis as a control 
agent by conducting basic and applied research on numerous insects and isolates (Dulmage and 
Beegle 1982). Critical to the use and commercialization of this organism was the development of 
standards for potency (Dulmage 1973 a and b). Strains and isolates of this organism are now used 
throughout the world to control many insect species. The development of application technologies 
was an important part of this program. Early studies on pathogens affecting insect pests of man and 
animals were initiated (e.g., Clark et al. 1968; Clark and O'Grady 1975; Hazard and Weiser 1968), 
and fungal and viral pathogens of mosquitoes were isolated (Chapman and Woodard 1966; Chapman 
et al. 1966). 


In the late 1960s and 1970s, ARS research led to a more thorough understanding of insect pathogens 
and their interactions with their hosts. Significantly more knowledge about their use was developed. 
Two morphological types of nuclear polyhedrosis viruses (NPVs) were discovered (Heimpel and 
Adams 1966) which led later to the discovery of a baculovirus having a broad host range and thus the 
potential to control several insect species (Vail et al. 1971). Control of a number of economically 
important insect species by viruses was demonstrated including Heliothis/Helicoverpa spp. (Ignoffo 
and Couch 1981), fall armyworm (Young and Hamm 1966; Hamm and Young 1971), gypsy moth, 
codling moth, cabbage looper and others (see Chapters III and IV). Field trials for the control of 
anopheline mosquitoes with Nosema algerae were conducted in Panama (Anthony et al. 1978). In 
1968, the ARS fire ant project began with a component for the development of microbial control 
agents (Knell et al. 1977; Avery et al. 1977; Jouvenaz et al. 1980; Banks et al. 1985). Significant 
reductions of grasshopper field populations by N. /ocustae were demonstrated (Henry 1971a). ARS 
scientists contributed significantly to the knowledge and development of in vitro cell cultures as 
related to entomogenous viruses, which greatly facilitated many studies on insect pathogens 
(Goodwin et al. 1970; Vaughn et al. 1977; see the additional references listed in Chapter IV, section 
B.3, and Appendix II). Numerous studies were conducted on the efficacy of B. thuringiensis 
israelensis. A number of UV screens were developed to reduce sunlight inactivation of microbial 
control agents (Ignoffo and Batzer 1971). This work continued into the 1990s with significant 
findings (Shapiro et al. 1992). Autodissemination of an insect pathogen was recommended for 
reduction of populations of khapra beetle (Burkholder and Boush 1974). 


At the beginning of the 1900s, the USDA was involved in one of the first attempts to use insect 
pathogens as classical biological control agents, targeting grasshoppers (Carruthers et al. 1997). In 
1919, the ARS European Parasite Laboratory was established in France. But it was not until 1981 
that an insect pathology program was initiated there to provide microorganisms for potential control 
of exotic pests in the U.S. The program gradually evolved, and a permanent position for insect 
pathology research was established in 1991 for on-site research at the European Biological Control 
Laboratory. In concert with the Laboratory, a Japanese beetle control program in the Azores Islands, 
Portugal, was recently implemented by ARS. However, the most significant development in the use 
of pathogens for classical biological control purposes has been the introduction by the USDA of the 
fungus Entomophaga maimaiga from Japan in 1910-12 and again in 1984-86 against the gypsy moth, 
which is proving to be an effective control agent for that pest (Reardon and Hajek 1993; Hajek et al. 
1995). Whether this can be claimed as a result of USDA’s introduction of the fungus is a debated 
issue; see Hajek et al. 1995. 


158 


In the late 1970s through the 1990s, basic and applied research on insect pathogens continued. 
Studies of pathogens of insects affecting man and animals led to the isolation and development of 
many pathogens for population suppression (Hazard and Weiser 1968). In-depth studies of a 
protozoan infectious to mosquitoes led to the landmark discovery that Thelohania in larvae and 
Nosema in adults were portions of the life cycle of one species (Hazard and Weiser 1968). A 
copepod was determined to be an essential intermediate host for a protozoan pathogen of mosquitoes 
(Sweeney et al. 1985). A South American protozoan pathogen from fire ants was isolated and 
described (Knell et al. 1977). After discovery of spiroplasmas at Beltsville by R. F. Whitcomb and R. 
E. Davis (Davis et al. 1972), scientists there demonstrated for the first time that these cell wall-less 
bacteria occurred in a number of insects in the orders Homoptera, Coleoptera, Lepidoptera, Diptera, 
and Hymenoptera (Clark 1982; Hackett and Clark 1989). 


As a result of ARS research, B. thuringiensis (Bt) was registered for use on stored grains and a 
granulosis virus also provided high levels of control (McGaughey 1983; Kinsinger and McGaughey 
1976). The first documented case of resistance to B. thuringiensis was described by McGaughey 
(1985) at the Manhattan, KS, Laboratory. Following the isolation of B. thuringiensis israelensis, 
formulations and application methods were developed for dispensing and applying the organism for 
control of aquatic Diptera, and standardized assay methods were developed (McLaughlin 1983; 
McLaughlin et al. 1984). Considerable research was conducted on a novel use of B. thuringiensis as 
a food additive to provide control of livestock pests in feces (Gingrich 1984). Temeyer (1984) was 
the first to demonstrate toxicity of the crystal protein of Bt to muscid flies. Considerable research 
effort was expended in developing Bacillus spp. for control of black flies during the 1980s (Lacey 
and Undeen 1984). 


As a result of increased databases, more microbial control agents were being field tested. Pressure to 
provide suitable alternatives to chemical insecticides was also a factor influencing increased field 
testing. Research was conducted with pathogens for area-wide suppression of multi-crop pests such as 
the cabbage looper (Vail et al. 1976) and Heliothis/Helicoverpa spp. (Bell 1988, 1990 a and b; Bell 
and Scott 1989; Bell et al. 1992). Adjuvants to increase the effectiveness of microbial pesticides were 
also developed (Bell and Kanavel 1978; Bell and Romine 1980; Hostetter et al. 1982; Dunkle and 
Shasha 1988; Bartell et al. 1990; McGuire et al. 1990; McGuire and Shasha 1990). Shapiro et al. 
(1992) discovered that high levels of synergism occurred between some of these compounds and 
baculoviruses. Gilliam et al. (1983) demonstrated that honey bees could be selected and bred for 
resistance to chalkbrood, and stressors were defined (Gilliam 1986). Captan was developed as an 
effective control for chalkbrood in leafcutting bees (Parker 1984, 1985, 1987, 1988; Mayer et al. 
1990). The world's foremost collection of entomopathogenic fungi was started by R. S. Soper and 
continued by R. A. Humber; over 3,200 isolates of over 250 species are in the collection (Humber 
1992). Intensive research on gypsy moth rearing and virus production resulted in the production of 1.5 
million insects in 100 days which yielded 50,000 acre treatment equivalents with a 10-fold reduction 
in production costs (Shapiro and Bell 1981; Podgewaite 1983). Nosema locustae was the first 
protozoan registered by the U.S. EPA. It was found that insect damage to raisins and other dried fruits 
could be minimized by the use of a granulosis virus (Hunter et al. 1977, 1979; Vail 1991). Simulation 
models were shown to be instrumental in guiding and evaluating studies on fungi infectious to 
grasshoppers (Larkin et al. 1988). Beauveria bassiana was found to move within corn plants and 
provide control of the European corn borer (Bing 1990; Bing and Lewis 1991; Lewis and Bing 1991). 
Stephen and Fichter (1990 a and b) successfully selected for resistance to chalkbrood in the alfalfa 
leafcutting bee. A rare protozoan was found to cause severe population reductions in the honey bee 
(Wilson and Collins 1992). 


Entomopathogens will likely be used even more in the future due to environmental and consumer 


concerns over chemical pesticides. ARS has been among the leaders in basic insect pathology and 
microbial control since the early 1900s. The strong research base provided by ARS and cooperating 


159 





research institutions should provide the basis to integrate insect pathogens into programs to manage 
insect pests in the future. 


160 


Table 7. Examples of Successful Classical Biological Control for which ARS and Predecessor 
Agencies Were Largely Responsible 


[Many other federal, state and university organizations and personnel (particularly University of 


California and APHIS-PPQ) were involved in some of these programs. Many examples of "partial" 
economic control cited above and in literature are not listed here. ] 


Type Pest Pest Species (Common Name) Crop Affected & Area of Control Chapter 


Reference 
Complete Economic Control 
Insects Cottonycushion scale Citrus - California I 
Citrus blackfly Citrus - Cuba I 
Citrus blackfly Citrus - Mexico II 
Comstock mealybug Fruits - Eastern U.S. Il 
European wheat stem sawfly Wheat - Eastern U.S. Il 
_}y Cereal leaf beetle Small grain - Eastern U.S. Il 
Alfalfa weevil Alfalfa - Eastern U.S. Il 
Rhodesgrass mealybug Range grass - Texas Il 
Pea aphid Alfalfa - U.S. Il 
Spotted alfalfa aphid Alfalfa - U.S. Il 
Alfalfa blotch leafminer Alfalfa - Eastern U.S. IV 
Eurasian pine adelgid Pine - Hawaii IV 
English grain aphid & Small grains - Chile IV 
Metopolophium dirhodum 
Weeds Common St. Johnswort Rangelands - Western U.S. II 
Tansy ragwort Rangelands - Western U.S. Il 
Alligatorweed Rivers, lakes - Southeastern U.S. Il 
Substantial Economic Control 
Insects Oriental, satin, gypsy, and Forest trees - New England I 
browntail moths 
Woolly apple aphid Apple - Northwestern U.S. I 
Alfalfa weevil Alfalfa - Western U.S. I 
Western pine tip moth Pine - Nebraska | 
Larch casebearer Larch - New England Il 
_-Oriental fruit fly Fruit - Hawaii Il 
Weeds Puncturevine Rangelands - Western U.S. Ill 
Musk thistle Pastures & rangeland - U.S. Ill 
Waterhyacinth Rivers, lakes - Southeastern U.S. IV 
Continued 


161 





Table 7. Examples of Successful Classical Biological Control for which ARS and Predecessor 
Agencies Were Largely Responsible--Continued 


[Many other federal, state and university organizations and personnel (particularly University of 


California and APHIS-PPQ) were involved in some of these programs. Many examples of "partial" 
economic control cited above and in literature are not listed here. ] 


Type Pest Pest Species (Common Name) Crop Affected & Area of Control Chapter 


Reference 
Potential Economic Control! 
Insects Plant bugs Alfalfa - Northeastern U.S. IV 
Birch leafminer Birch - Northeastern U.S. IV 
Euonymus scale Ornamentals - U.S. IV 
Weeds Yellow starthistle Rangelands - Western U.S. IV 
Leafy spurge? Rangelands - Western U.S. IV 
Purple loosestrife’ Wetlands - Northern U.S. IV 


' Programs are too recent to predict complete economic control, but preliminary results indicate at 
least substantial control will result. 


* Agriculture Canada and International Institute for Biological Control are much involved in the 
potential success of this program. 


* ARS involvement chiefly limited to initial stages of this program. 


162 


Table 8. ARS Scientists Devoted Full or Half Time to Classical Biological Control - December, 
1993 


[Based on personal count, not Research Management Information System (RMIS) accounting, for 
which, see text; does not include 1 SY in Biological Control Documentation Center, Beltsville, MD.] 


Location Target 

Arthropod Pests Weeds 

Agent Agent 
Parasites and § Pathogens Pathogens Invertebrates 
Predators 

Europe Ehebeb 1.0 SY 3.5 SY 0 
South America 0.5 SY 0 0.5 SY 0 
Australia 0 0 LOY: 0 
Asia 0 0 0 0 
NE U.S 3.5 SY- 0 0 35S ie 
SE U.S. 05 SY 0 20:5 ¥5 0 
NC U.S 0 0 0 0 
W US. LS: Sy 0 ieee LoS Ye 
TOTALS eeaCp 1.0 SY ihe saeloty € S,0:5%, 





' Funded by "soft" funds (see text) 

? Newark, DE (3); Beltsville, MD (0.5) 

3 Frederick, MD (only 2 full time) 

4 Stoneville, MS 

> Gainesville, FL (1); Fort Lauderdale, FL (1) 

® Sidney, MT (0.5; "soft" funds); Yakima, WA (0.5); Stillwater, OK (0.5) 
7 Bozeman, MT (1.5); Sidney, MT (1); Albany, CA (1); Temple, TX (2) 
§ Bozeman, MT 


163 


Table 9. Estimated Resources Devoted to all Types of Biological Control by the Agricultural 
Research Service, 1987 


Scientist Years (SY) and $ (000's) 


Biological SYs' FY 1988! FY 1989 
Control Agent Estimated Estimated Estimated 


Target: Arthropod Pests (Insects, Mites, and Ticks) 


Arthropod 

Parasites (Parasitoids) 41.2 $ 6,180 $ 6,180 
Predators 175 2,625 2,625 
Pathogens 315 Aw25 4.725 
Parasitic Nematodes 4.] 615 615 
SUBTOTAL 94.3 14,145 14,145 

Target: Weed Pests 
Phytophagous Arthropods 15.8 2,370 2,370 
Phytophagous Nematodes 0.0 0 0 
Mycoherbicides 8.3 1,245 1,245 
Plant Allelopaths 2s 375 BIS 
Herbivorous Fish 0.2 30 30 
SUBTOTAL 26.8 4,020 4,020 
Target: Plant Pathogens and Nematodes 

Microbial Antagonists 21.6 3,240 3,240 
Nematophages 1.0 150 150 
SUBTOTAL 22.6 $ 3,390 $ 3,390 
GRAND TOTAL 143.7 $21,555 $21,555 


———_—_—_—_—s—o——osos—"“<S—amnys—a—X—s—S——————— 


' Based on a survey conducted in May 1987, as reported in King et. al. 1988. Figures have not been 
updated. 


164 


Table 10. Estimated Scientist-Years Devoted to all Types of Biological Control in the 
Agricultural Research Service, 1987 


Biological Control Research to Protect Selected Commodities/Areas from Pests 


Commodity/Area Control Approach (SYs)' Total 
Classical Conservation Augmentation SYs Scientists 

Plants 

from Arthropods 18.0 14.2 41.8 74.0 120 

from Weeds/Brush 15.9 1.3 6.8 24.0 40 

from Disease 0.6 4.2 14.8 19.6 36 

from Nematodes 0.1 0.3 0.7 1.1 2 

Aquatic Resources 

from Weeds 2,1 0.0 0.1 2.2 3 

Man/Animals 

from Arthropods 6.1 1.1 4.7 11.9 ee 

Post-Harvest Products 

from Arthropods 0.6 0.6 6.5 7.7 16 

from Pathogens 0.0 0.3 1.8 21 5 

TOTAL SYs 43.4 22.0 a7c2 142.6 

TOTAL SCIENTISTS 84 74 148 7218 





' Based on a survey conducted in May 1987, as reported in King et. al. 1988. Figures have not been 
updated. 


? Scientists often conduct research across several commodities/areas or control approaches, and thus 
total in this column exceeds 218. 


165 


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258 


APPENDIX | 
DOCUMENTS CITED IN CHAPTER IV 


259 


A. CHARTER OF THE ARS WORKING GROUP ON NATURAL ENEMIES OF INSECTS, 
WEEDS, AND OTHER PESTS (WGNE) 


During the May 1973 meeting of the ARS Board of Directors, a Plan for the WGNE was approved, 
and its membership appointed. The following is a copy of this Plan as slightly revised following the 
first WGNE meeting in October 1973. 


A PLAN 
COORDINATION AND LEADERSHIP OF 
BIOLOGICAL CONTROL RESEARCH 
IN THE 
AGRICULTURAL RESEARCH SERVICE 


INTRODUCTION 


The concept of biological control of pests involves the discovery, identification, evaluation, 
introduction and establishment of highly specific natural enemies (parasites, predators and 
pathogens) of target insects, weeds, nematodes, plant pathogens and other pests. It also involves the 
development of technology essential to manipulating such exotic and native enemies toward a 
balance which favors the plant, animal and beneficial organisms important to man's well-being and 
survival. 


An effective and efficient program for biological control of pests is contingent on a manageable and 
productive multidiscipline research and development effort. The current program of ARS involves 
many scientists studying various aspects of biological control at foreign and domestic locations, as 
indicated in the attached appendix. 


Since biological control studies encompass a complex network of research programs in several 
foreign centers and a widely diverse set of environmental conditions in the United States, a 
mechanism is hereby created to facilitate coordination and cooperation among the various locations 
and groups in ARS and with outside cooperators and interested agencies. 


AGENCIES AND ORGANIZATIONS COOPERATING 
IN BIOLOGICAL CONTROL RESEARCH 


The research on biological control of insects, weeds and other pests is of special interest to many 
other federal and state agencies. Some of these agencies support the cooperative ARS research 


program financially and utilize the biological agents in their insect, weed and other pest management 
programs. 


Federal agencies concerned are the Departments of Defense, Interior, Agriculture, and Health, 
Education and Welfare, and the independent agencies -- Environmental Protection Agency and 
Tennessee Valley Authority. State Agricultural Experiment Stations, State Departments of 

Agriculture and state agencies responsible for water management are frequently cooperators in 


260 


biological control programs. In addition liaison is maintained with the Commonwealth Institute of 
Biological Control and counterpart agricultural agencies in Canada and Mexico. A high degree of 
coordination with these various agencies at the state, national and international levels is essential to 
the attainment of efficiency and effectiveness of the overall research program on biological control. 


PLANN AND COORDINATION OF RESEARCH 


Authority for planning and coordinating a national program for biologcal control research is vested in 
the National Program Staff and the ARS Working Group on Natural Enemies of Insects, Weeds and 
Other Pests. 


ARS Working Group on Natural Enemies of Insects, 
Weeds, and Other Pests (WGNE) 


(a) Composition - The Assistant Administrator of ARS for Plant and Entomological Sciences shall 
appoint the Chairman and Cochairman to this Working Group. Both the Chairman and 
Cochairman will be members of the National Program Staff for Plant and Entomological 
Sciences. Other NPS members will participate as the situation requires. Appropriate members 
from each Region will be appointed by the Deputy Administrators. The Administrator will 
designate a member from the International Programs Division. Depending on the program under 
consideration, the Chairman can request participation by one or more biological control 
specialists who are not members of WGNE. 


(b) Function 


- To complete periodic reviews of both the domestic and foreign research on biological control 
within ARS in light of national needs and goals. 


- To recommend the establishment of coordinating subgroups* and research teams* as 
appropriate to work on interregional biological control problems. The composition of 
subgroups and research teams will be identified together with special funding requirements. 
[* See below. ] 


- To prepare reports when needed for the Administrator on the priority needs and goals of 
biological control research. The reports will include: (a) proposals on major shifts in 
resources, both personnel and funds, to meet high priority needs, and (b) recommendations 
for the establishment of coordinating subgroups and research teams to facilitate interregional 
research needs, and (c) other recommendations as required. 


(c) Procedures 


A substantial portion of ongoing research will not require establishment of formal guidelines 
for cooperation within and between regions. However, coordinating subgroups and research 
teams will be organized to fulfill national needs for biological control investigations. 


- Coordinating subgroups will be named and chairmen selected where there is an identifiable 
need for periodic planning and reporting sessions for specialists working on a common 
problem. Thus, subgroups would serve a useful role in the identification of target pests for 
biological control work within different Regions and coordinating the receipt, propagation, 
distribution, release and evaluation of effectiveness of the agents as components of balanced 
insect and weed management programs. 


261 


- Research teams will be named for high priority research projects that demand close 
coordination and direction. The team will assume a direct coordinating role for the life of the 
research project. In this capacity, it will exercise responsibility over the technical direction of 
personnel and the coordination of resources assigned to the project as mutually agreed upon 
by the parties concerned in advance. 


- Chairmen of coordinating subgroups and research team leaders are responsible to their 
respective Area Directors. Reports will be prepared as needed. The WGNE evaluates 
progress, establishes priorities, recommends modification in plans and approves continuation 
of subgroups and research teams. 


- The Adminstrator, ARS, will give final approval to the establishment of and appointment to 
coordinating subgroups and research teams. 


[There followed an Appendix listing the major biological control units within ARS as determined at 
that time, with statements as to the major activities conducted by each, and whether quarantine 
facilities were available at that location. Because major changes have occurred since 1973, only the 
names of the units and their locations are listed here. For more up-to-date lists of ARS biological 
control units, see Coulson and Hagan 1986, and the "Profiles of ARS Biological Control Scientists" 
in King et al. 1988.] 


262 


MAJOR BIOLOGICAL CONTROL RESEARCH UNITS WITHIN ARS [in 1973] 
Overseas Laboratories 


1. Biological Control of Weeds Laboratory, Rome Italy 
2. Biological Control of Weeds Laboratory, Buenos Aires, Argentina 
3. European Parasite Laboratory, Sevres, France 


Domestic Laboratories 


Western Region 


1. Cotton Insects Biological Control Laboratory, Tucson, AZ 

2. Western Cotton Research Laboratory, Phoenix, AZ 

3. Biological Control of Weeds Laboratory, Albany, CA* 

4. Western Insects Affecting Man and Animals Laboratory, Fresno, CA 
5. Stored Product Insects Research Laboratory, Fresno, CA 

6. Grasshopper Laboratory, Bozeman, MT 


Northeastern Region 


1. Potato Insects Investigations, Orono, ME 

2. Beneficial Insects Research Laboratory, Newark, DE* 

3. Plant Disease Research Laboratory, Frederick, MD* 

4. Systematic Entomology Laboratory, Beltsville, MD 

5. Beneficial Insect Introduction Laboratory, Beltsville, MD 
6. Insect Pathology Laboratory, Beltsville, MD 
7. Nematology Laboratory, Beltsville, MD 


North Central Region 


1. Biological Control of Insects Research Laboratory, Columbia, MO 


Southern Region 
1. Cotton Insects Research Laboratory, College Station, TX 
2. Entomology Research Center, Brownsville, TX 
3. Gulf Coast Mosquito Research Laboratory, Lake Charles, LA 
4. Special Plant Feeding Insect Quarantine Facility, Stoneville, MS* 
5. Bioenvironmental Insect Control Laboratory, Stoneville, MS 
6. Southern Weed Science Laboratory, Stoneville, MS 
7. Southern Grain Insects Research Laboratory, Tifton, GA 
8. Tobacco Research Laboratory, Oxford, NC 
9. Aquatic Weed Control Laboratory, Fort Lauderdale, FL 
10. Biological Control Laboratory, Gainesville, FL* 
11. Insects Affecting Man Research Laboratory, Gainesville, FL 
12. Insect Attractants, Behavior & Basic Biology Laboratory, Gainesville,FL 


*Quarantine facility available 


Initial 1973 membership of WGNE included the following persons: 


W.B. Ennis, NPS, Chairman 
M. D. Levin, NPS, Cochairman 


Northeastern Region North Central Region 
J. R. Coulson C. M. Ignoffo 

A. M. Heimpel L. A. Bulla 

Southern Region Western Region 

R. L. Ridgway D. E. Bryan 

C. R. Swanson L. A. Andres 


International Pr ms Divisi 
Not determined 


263 


B. CHARTER OF THE WORK GROUP ON BIOLOGICAL PEST CONTROL AGENTS 


(WGBCA) 
OFFICE OF ENVIRONMENTAL QUALITY ACTIVITIES 
Office of the Secretary 
U.S. Department of Agriculture 
WORK GROUP ON BIOLOGICAL PEST CONTROL AGENTS 
Charter 
BACKGROUND: 


Biological pest control is a critical element in moving toward a total strategy for pest control. It 
involves the efficacious use of parasites, predators, and microorganisms, to control insects, 
nematodes, weeds, and pathogen pests on animal and plant hosts. The effectiveness of biological 
control can be assessed on the basis of economic as well as environmental benefits within the 
complex of pest control strategies. 


At this time there is need for an improved understanding of adequate research and proper research 
balance, the development and implementation of effective biological control programs, and the 
establishment of legislative authority necessary for using certain types of biological controls. From 
the regulatory viewpoint, jurisdictional responsibilities need further clarification. It is appropriate for 
the Department to cooperate with the States and private organizations to utilize expertise on 
biological controls required to identify specific issues, assess the implications of these issues, and 
recommend possible courses of action that can contribute to development of sound programs and 
policy and regulatory requirements. 


ORGANIZATION AND PURPOSE: 


To provide for multi-agency and interdisciplinary participation in developing recommendations 
regarding programs and policies required to further promote biological pest control research and 
implement biological control programs, there is established a Work Group on Biological Pest Control 
Agents under authority of Secretary's Memorandum 1890, dated January 7, 1976. This effort is 
intended to assist in realizing the full potential of biological control to pest control activities. The 
roles of the Work Group include coordination and information exchange as contrasted to program 
leadership or management. The Work Group will provide background for Departmental situation 
assessment, problem identification, and identification of potential problem-solving approaches. 


The Work Group will consist of a Chairman and appropriate representatives from involved USDA 
agencies. It will be responsible to the Office of Environmental Quality Activities. The membership is 
shown on Attachment #1 [not included here]. 


Member Agencies: ARS, APHIS, CSRS, ERS, ES, FS, OGC. 


264 


OBJECTIVES: 


1. Evaluate the current status of biological control research and implementation activity, 
including an appraisal of past research implementation and success. 


2. Coordinate the evaluation of emerging research and development needs. 


3. Coordinate the evaluation of economic, biological, environmental and legislative 
implications of past and potential research and implementation programs. 


4. Identify policy issues, implications of the policy issues and alternative courses of action to 


provide for further development and implementation of biological controls within a system of pest 
control strategies. 


5. Recommend formation of task forces, as required, to develop in-depth analyses of specific 
subject-matter. 


265 


C. MEMORANDUM OF AGREEMENT BETWEEN USDA AND CALIFORNIA, 1974 REVISION 


No. 3855 
MEMORANDUM OF AGREEMENT 

Among 

THE REGENTS OF THE UNIVERSITY OF CALIFORNIA 

THE CALIFORNIA STATE DEPARTMENT OF FOOD AND AGRICULTURE 
And 
THE UNITED STATES DEPARTMENT OF AGRICULTURE 
AGRICULTURAL RESEARCH SERVICE 
ANIMAL AND PLANT HEALTH INSPECTION SERVICE 


THIS AGREEMENT is entered into by and among The Regent of the University of California, a 
California Corporation, hereinafter called "The Regents", the State of California acting by and 
through the California Department of Food and Agriculture, hereinafter called "The State", and the 
United States Department of Agriculture, Agricultural Research Service, hereinafter called ARS, and 
Animal and Plant Health Inspection Service, Plant Protection and Quarantine, hereinafter called the 
Service. 


WHEREAS, the parties hereto desire to provide hereby an outline of a general procedure under 
which they will operate in a cooperative project whereby beneficial insects and other organisms are 
to be imported into the State of California from localities outside the continental United States as an 
aid in the biological control of pests affecting agriculture within the State; and 


WHEREAS, the parties hereto desire that this agreement replace and be substituted in lieu of the 
Memorandum of Agreement among the parties, dated January 14, 1964, and covering the subject 
matter of this agreement. 


NOW, THEREFORE, the parties hereto agree as follows: 

A. The Regents Agree: 
1. To provide and maintain a quarantine facility adequate to prevent the escape of any 
beneficial insect or other insects or organisms which may be imported by State or Regental 
agencies. 
2. That prior to the use of any quarantine facility, it shall be approved in writing by duly 
authorized representatives of the Service; and if specifically requested, by duly accredited 


representatives of other contracting agencies. 


3. That all shipments of beneficial insects and other organisms shall be opened only in a special 
room to be known as a "quarantine room"; this room shall be approved in the same manner as 


266 


provided above and shall be so screened or otherwise safeguarded to preclude the escape of 
insects or other organisms and shall be so constructed as to permit effective disinfection. 


4. That all containers and packing material shall be destroyed after the insects or other 
organisms have been removed therefrom; provided, however, the standard containers of a more 
or less permanent nature may be fumigated or otherwise treated in a manner which will insure 
their freedom from any kind of living insect or organism. 


5. That the quarantine room and other rooms in which the insects or other organisms are studied 
shall at all times be kept under lock and only those employees who are authorized by the 
Director of the Agricultural Experiment Station, University of California, or by a designated 
representative shall have access to such room or rooms. 


6. Shipments of beneficial insects and other organisms consigned to the United States 
Department of Agriculture or the State may be processed in The Regents quarantine facilities 
upon written approval of The Regents. 


7. That an accurate record shall be maintained of all importations and at appropriate intervals, 
and in any event not less frequently than six months, a report of progress of work and/or 
conditions of imported material shall be sent to the other parties to this agreement. 


8. That interstate shipments of living imported species or varieties of insects or other organisms 
shall be made only upon approval of the Service. 


It is Mutually Understood and Agreed: 


1. That all importations, by any party hereto, into California from points outside the continental 
United States of any beneficial insects or other organisms shall be approved and agreed to in 
writing, in advance, by all parties to this agreement. 


2. That The Regents and the State shall be advised, in writing, prior to execution, of all 
importations undertaken solely by the ARS and the Service and dealing with the direct 
importation into California of beneficial insects or organisms intended primarily for ultimate 
liberation within the State. 


3. That no importations of beneficial insects or other organisms shall involve the entry into 
California of (a) plants which are hosts of citrus canker; (b) fruits or vegetables which serve as 
hosts of the Mediterranean fruit fly or related fruit flies from countries where such pests are 
known or believed to occur; or (c) hosts of injurious pests not known to occur in or to be widely 
distributed within the United States from localities where such pests are known or believed to 
occur, with such exceptions as may be agreed upon in writing by the parties to this agreement. 


4. That the Director of the Agricultural Experiment Station of the University of California shall 
be in charge of and have supervision over all material with research potential imported by the 
State or the Regents under this agreement until necessary investigations are completed to 
determine the results of such importations. If satisfactory results are obtained from any 
importation, the progeny from such importation, after due written notice to the parties to this 
agreement, may be distributed by the Director, or a designated representative to other 
institutions or individuals believed to be competent and equipped to rear and/or liberate such 


progeny. 


267 


268 


5. That all materials to be imported under this agreement shall be entered only on permits 
issued by the Service and copies of all applications for permits and copies of all permits so 
issued shall be furnished to the State. 


6. That those imported shipments of beneficial insects or other organisms under this agreement 
which the State requires to be inspected shall be received and examined at the port of first 
arrival by authorized representatives of the Service, and such inspections shall be confined to 
such examination of the containers as may, in the judgement of the inspector, be necessary to 
determine that they are sufficiently secure and in such condition as will assure safe arrival at the 
designated quarantine facility. These shipments will be forwarded to the designated quarantine 
facility as expeditiously as possible. 


7. That initial liberations of phytophagous organisms imported under this agreement shall be 
made in California only after written approval of the parties to this agreement. Subsequent 
liberations of progeny from the importations made under a given permit shall not need 
additional approval by the parties to this agreement. Such liberations shall continue to be 
recorded and reported in accordance with paragraph A.7 of this agreement. 


8. That this Memorandum of Agreement is to define in general terms the basis on which the 
parties concerned will cooperate, and does not constitute a financial obligation to serve as a 
basis for expenditures. Each party will handle and expend its own funds. Any and all 
expenditures from federal funds in the U. S. Department of Agriculture made in conformity 
with the plans outlined in this Memorandum of Agreement must be in accord with the 
Department's Rules and Regulations and in each instance, based on appropriate finance papers. 
Expenditures made by The Regents of the University of California and the California State 
Department of Food and Agriculture, will be in accord with their Rules and Regulations. Funds 
of a cooperating party shall not be expended by a federal employee even though the cooperating 
party has no representatives stationed in the locality. In such cases, a federal employee may 
handle the accounts but shall forward the vouchers to the authorized agent of the cooperating 
party for payment. Cooperating parties should not send checks payable to federal employees or 
send them checks payable to "Cash" or "Bearer" for payment of local expenses. 


9. That the responsibilities assumed by the cooperating parties are contingent upon funds being 
available from which the expenditures legally may be met. 


10. No member of or delegate to Congress, or resident commissioner, shall be admitted to any 
share or part of this agreement or to any benefit that may arise therefrom, unless it be made with 
a corporation for its general benefit. 


11. This Memorandum of Agreement represents a revision and supersedes the present 
agreement, which was effective January 14, 1964. 


12. That this agreement shall become effective upon date of final signature and shall continue 
indefinitely, but may be modified by mutual agreement among the parties in writing and may be 
discontinued at the request of any of the parties. Request for termination or of major change 
shall be submitted in writing to the other parties not less than sixty (60) days in advance of the 
effective date desired; provided, that such termination shall not become effective until 
arrangements reasonably satisfactory to the other parties have been made for the destruction or 
other disposition of any materials, organisms or specimens which have been imported into 


California under this agreement and which, at the time of such termination are being used in 
laboratory tests or experiments. 


CALIFORNIA STATE DEPARTMENT OF FOOD 
AND AGRICULTURE 


signed: C. B. Christensen 
Director 


THE REGENTS OF THE UNIVERSITY OF 
CALIFORNIA 

igned: J. B. Kendrick 
Vice President, Agricultural Sciences Director, 
Agricultural Experiment Station 


UNITED STATES DEPARTMENT OF 
AGRICULTURE AGRICULTURAL RESEARCH 
SERVICE 


signed: Gail F. Sedgwick 
Acting Administrator 


UNITED STATES DEPARTMENT OF 
AGRICULTURE ANIMAL AND PLANT 
HEALTH INSPECTION SERVICE 


signed: E. E. Norris 
Acting Administrator 


NOV 25 1974 
Date 


269 


APPENDIX II 
DETAILED HISTORY OF INSECT PATHOLOGY RESEARCH 
IN THE AGRICULTURAL RESEARCH SERVICE, 
ARRANGED BY LOCATION 
Edited by P. V. Vail 


The United States Department of Agriculture (USDA) has been involved in insect pathology and 
microbial control research since the early 1900s. Some of the early projects such as those for 
Japanese beetle and diseases of the honey bee provided the stimulus for modern day research 
programs and the acceptance of insect pathology and microbial control as distinct disciplines. Many 
of the basic research findings of the Agricultural Research Service (ARS) in these disciplines have 
provided the information necessary to develop both microorganisms as control agents and control 
methods for insect diseases in pest and beneficial species and also have found use in other disciplines 
such as medicine. This document was prepared by research scientists from most of the past and 
current ARS laboratories conducting research in insect pathology and microbial control. It describes 
research on insects of importance to food and crops, man and animals, and forests. The collection of 
histories provides the reader with research accomplishments and pertinent literature. The collection 
of histories is current through 1992. They are arranged alphabetically by state and country in which 
the research was conducted; see main Table of Contents. 


As in other parts of this book, the full scientific name and taxonomic hierarchy of all organisms 
discussed in the text of this Appendix are cited only in the Index, where they are cross-referenced 
with the common name, if used in the text. 


Acknowledgment: The editor expresses his sincere gratitude to Ms. Elisabeth Nye Fouse and Ms. 
Darlene Hoffmann, USDA-ARS Horticultural Crops Research Laboratory, Fresno, CA, the former 
for assistance and perseverance in typing, editing and organizing this document, the latter for 
assistance with the literature search, and to Dr. Martha Gilliam, USDA-ARS Carl Hayden Bee 
Research Laboratory, Tucson, AZ, and Dr. Leslie C. Lewis, USDA-ARS Ankey, IA, for reviewing 
the manuscript. 


WESTERN VEGETABLE AND SUGAR BEET INVESTIGATIONS LABORATORY, MESA, AZ: 
By Patrick V. Vail 


In 1969, P.V. Vail joined the staff of the Western Vegetable and Sugarbeet Investigations Laboratory 
in Mesa, AZ, as Investigations Leader and centered his studies on microbial control of lepidopterous 
pests of vegetables with entomogenous viruses. While at the Mesa laboratory, Vail explored the host 
range of the nuclear polyhedrosis virus (NPV) isolated from alfalfa looper (AcMNPV) (Vail et al. 
1973b). These early studies showed that the cotton leafperforator (Vail et al. 1971a), the pink 
bollworm (Vail et al. 1972b), and diamondback moth (Vail et al. 1972a) were also susceptible to this 
virus. Extensive histopathological studies were also conducted on a number of the alternate hosts of 
AcMNPV (Vail and Jay 1973). Vail et al. (1973b) were the first to show extensive complete and 
rapid replication of a baculovirus in an insect cell line. Occluded virus was as infective as in vivo 


270 


produced virus. Later, Hink and Vail (1973) developed the first plaque assay for an 
entomopathogenic virus using the same cell line-virus system. 


Methods of mass producing noctuid larvae, their parasitoids and viral pathogens were also 
investigated. Several different larval diets and virus production methods were developed that 
provided high yields and minimized labor (Vail et al. 1973a). Several large-scale field tests were 
conducted near Tucson, AZ, demonstrating the feasibility of using several baculoviruses and Bacillus 
thuringiensis for control of the cabbage looper on lettuce (Vail et al. 1972c). The influence on 
parasitoid and predator populations was also determined. Later Vail et al. (1980) conducted further 
tests on the use of several NPVs and spray adjuvants for the control of cabbage looper infesting 
lettuce in Arizona. Also the merits of reducing cabbage looper populations on cotton with a 
baculovirus before it moves into lettuce was demonstrated (Vail et al. 1976b). These tests provided 
the first information that indicated area-wide suppression of an agricultural pest with a baculovirus 
might be feasible. Insects could be controlled on one crop or alternate host to reduce infestation in 
another possibly higher value crop. 


As NPV infections were often found associated with the parasitoid Voria ruralis parasitism in mass- 
rearing systems, studies were conducted to determine if the parasitoid was responsible for virus 
transmission. Conversely, parasitism rates by V. ruralis were often masked by parasitoid larvae dying 
within diseased hosts prior to completion of development. At times V. ruralis larvae were found only 
in diseased larvae. Because of the long pre-oviposition period most of the virus acquired by the 
parasitoid while in the host was voided prior to the time the parasitoid was capable of parasitization 
(Vail 1981). Polyhedra were found in the midgut of parasitoids emerging from NPV-infected larvae. 
Viable polyhedra could be found in the meconia and adult feces. However, the infectivity of adult 
homogenates was quite low indicating that any virus in the adults was voided soon after emergence. 
The infectivity could be demonstrated for only several days after emergence. Thus it was 
demonstrated that adult parasitoids could act as mechanical vectors for short periods of time. Voria 
ruralis adults could help distribute virus inoculum to other sites under natural conditions. The 
possibility of host feeding as a means of virus transmission/dissemination was not investigated. In 
1971, Vail transferred to the Western Cotton Research Laboratory in Phoenix, AZ. 


WESTERN COTTON RESEARCH LABORATORY, PHOENIX, AZ. By Marion R. Bell and 
Patrick V. Vail 


P.V. Vail and M.R. Bell conducted insect pathology/microbial control research at the Western Cotton 
Research Laboratory in Phoenix from 1971 to 1985. In 1971, Vail transferred to the Laboratory as 
Research Leader for cotton insects investigations. Vail continued to conduct research on in vitro 
production of the alfalfa looper NPV (AcMNPV) using modified media (Vail et al. 1976a). The 
impact of applications of AcMNPV on cotton leafperforator was also demonstrated (Vail et al. 
1977a). As a result of ARS Pilot Test funding Vail et al. (1977b) evaluated several techniques as 
components of an integrated system for control of pink bollworm in the Southwest. Using 
commercial type applications, AcMNPV was found to have little effect on pink bollworm 
populations, although infected larvae were obtained from treated plots. Vail et al. (1979), in 
cooperation with the ARS Insect Pathology Pioneering Research Laboratory, Beltsville, MD, 
demonstrated the in vitro infectivity of AcMNPYV liberated from polyhedra with digestive juices. This 
finding led to a potential alternative method to the commonly used alkali liberation techniques. Vail 
et al. (1989) also determined quantitatively the residues of AcMNPYV after field applications to 
cotton. A high correlation between residues and infection levels of cotton leafperforator populations 
was demonstrated. In 1975, Vail took a leave of absence to take a position with the International 
Atomic Energy Agency in Vienna, Austria. 


294 


Bell transferred from the Boll Weevil Research Laboratory, Mississippi State, MS, in 1972. He 
developed a technique for determining the feeding preference of newly-hatched pink bollworm larvae 
and used the method to develop a formulation which increased the effectiveness of pathogens 
(Bacillus thuringiensis (Bt) and baculoviruses) in laboratory and field studies. This research 
established that newly-hatched pink bollworm larvae could exhibit a feeding preference, and that the 
feeding behavior could be modified on cotton by the presence of these cotton-based feeding 
materials. Results of the field study demonstrated that cotton-based adjuvants increased the 
effectiveness of baculovirus against Heliothis spp. (sens. lat.) but failed to significantly affect 
efficacy for pink bollworms. The study also suggested a new method of insect control: the 
application of materials which elicit feeding in or on less important plant parts and which reduce the 
pest population by altering feeding habits. The materials identified in this study were further 
modified by Bell for cooperative studies with H.M. Flint (USDA-ARS, Phoenix) and P.D. Lingren 
(USDA-ARS, Lane, OK) for possible use in pink bollworm pest management programs, and R.T. 
Staten (USDA-APHIS, Phoenix) for possible use in a boll weevil program (Bell and Kanavel 1975, 
1977a). Bell and Kanavel (1976) conducted basic investigations into the host-pathogen relationship 
between the pink bollworm and its cytoplasmic polyhedrosis virus (CPV). These studies described 
the relationship between dose, growth, and mortality, and viral effects were described which were 
previously unknown. This knowledge helped in his participation as a cooperative member in a team 
of ARS/APHIS personnel working to control this pathogen in a pink bollworm mass rearing facility. 
The clean-up procedures resulted in a 5-fold production increase (Bell and Kanavel 1976, 1977b; 
Stewart et al. 1976; Bell 1977). 


Through a sequence of laboratory, greenhouse, and field research studies, Bell developed a practical 
feeding adjuvant (COAX™) that increased the effectiveness of pathogens as well as other 
insecticides in pest control programs. He conducted the research necessary to demonstrate its 
commercial possibilities and aided Proctor and Gamble, Inc., to develop a commercial product. This 
product reached annual sales of $15 million. The development of new chemical insecticides (i.e., 
pyrethroids) for cotton insect control decreased the quantity of product marketed. However, the 
insect management technique and product developed remain as a viable and efficacious alternative 
for Heliothis (sens. lat.) control in cotton, and continue to be used in limited areas of the U.S. and 
foreign countries. COAX™ has also been studied by many domestic and foreign scientists and 
shown to be effective in a variety of insect control programs (e.g., control of Spodoptera and 
Helicoverpa armigera in Israel) (Bell and Kanavel 1978; Bell and Romine 1980). 


With the technical assistance of C.L. Romine, Bell conducted field studies to determine the potential 
of two microbial insecticides for control of cotton leafperforator. Results showed that a bacterium 
and virus mixture was effective in preventing damage. Since these pathogens had already proven 
useful in the control of Heliothis (sens. lat.) in cotton, their usefulness in the control of the cotton 
leafperforator provided further evidence for their use in pest management programs (Bell and 
Romine 1982). 


Bell conducted laboratory experiments to study the effects of mixtures of the bacterium Bacillus 
thuringiensis and nuclear polyhedrosis viruses on several lepidopterous pests. The results of these 
tests aided in the understanding and evaluation of these pathogens when used under field conditions. 
Several important sublethal dosage effects were discovered during this research which could be very 
important to integrated pest management programs utilizing microbials. For example, a method of 
using prophylactic treatments of low, sublethal applications of B. thuringiensis is being used 
successfully by some growers (Bell and Romine 1986). 


212 


BEE RESEARCH LABORATORY, TUCSON, AZ. By Martha Gilliam 


Martha Gilliam was awarded an ARS Cooperative Agreement Grant while at the University of 
Arizona to conduct research on immune mechanisms of the honey bee (Gilliam 1973). Part of this 
work involved Bacillus larvae, the causative organism of American foulbrood disease (AFB). The 
results showed that agglutinating substances are produced and disseminated rapidly within the body 
of the adult worker honey bee in response to an injection of a vaccine prepared from B. larvae 
(Gilliam and Jeter 1970). 


In 1969, Gilliam received a Civil Service appointment as a Microbiologist at the ARS Bee Research 
Laboratory of the Carl Hayden Bee Research Center at Tucson. Her primary assignment was to 
define the normal microflora (bacteria, yeasts, and molds) of honey bees, their food (pollen and 
nectar), and environment and then to determine microbial contributions to honey bee nutrition, 
biochemistry, and physiology. 


Gilliam began long-term cooperative research efforts with several scientists. Stephen Taber III, a 
Research Entomologist who preferred the title Apiculturist, retired from the Carl Hayden Bee 
Research Center in 1979. He and Gilliam continued to work together after his retirement. Dorothy 
Prest, a mycologist at Keuka College, New York, began working with Gilliam in 1971. After her 
retirement in 1984, she moved to Tucson and has been a Collaborator at the Carl Hayden Bee 
Research Center since then. L.J. Wickerham, the noted yeast taxonomist, retired from the ARS 
Northern Regional Research Laboratory in Peoria, IL, and was a collaborator at the Carl Hayden Bee 
Research Center from 1974-1985. Gilliam also has worked for many years with Robert Argauer, 
Research Chemist, ARS, Beltsville. 


Results from the normal flora project obtained over 18 years were summarized by Gilliam (1989). It 
was shown that healthy honey bee eggs, prepupae, and pupae are free internally of microbes. Larvae 
can be inoculated with microbes from ingestion of contaminated food, but these are usually 
eliminated through defecation at the end of the feeding period. Emerging adult worker bees generally 
have no intestinal microflora until they are inoculated by trophallaxis and pollen consumption. 
Nectar contains few or no microbes. 


Microflora of honey bees are dominated by Gram-variable pleomorphic bacteria, Bacillus spp., 
Enterobacteriaceae, Penicillia, and Aspergilli. Yeasts in bee intestines appear to be indicators of 
stress and are represented most frequently by Torulopsis spp. Ingestion of antibiotics used to control 
bee diseases, certain pesticides, and caging of both colonies or bees alters the intestinal microflora. 
Digestive enzymes in honey bees originate from the bees themselves, from pollen, and from 
micoorganisms. 


Microbiological examination of various organs of mated and virgin queen honey bees revealed that 
yeasts rarely occur in queen bees, and molds occur less frequently in the guts of queen bees than in 
those of worker bees. Bacteria belonging to the genus Bacillus are present, although Gram-negative 
rods and Gram-variable pleomorphic bacteria were more numerous. The antimicrobial properties of 
royal jelly that is seemingly the diet of the queen bee throughout her entire life may prevent many 
microorganisms from becoming established in the gut. In contrast, pollen that is consumed by worker 
bees and food obtained from other bees in the colony are the primary sources of inocula for the gut 
microflora of this caste. 


Pollen is the chief dietary source of proteins, amino acids, lipids, vitamins, and minerals for honey 


bees. Foraging bees collect pollen that is then packed into the comb cells of the brood comb. This 
store of pollen, which has undergone chemical changes, is called bee bread. 


273 


Studies on the microbiology of floral and corbicular pollen and of bee bread stored in comb cells of 
the hive demonstrated that pollen from a flower changes both biochemically and microbiologically as 
soon as a bee collects it due to the addition of secretions and microbes which produce and conserve a 
nutritive product for consumption. Molds, yeasts, and Bacillus spp. are the predominant microbes in 
pollen and bee bread. It appears that bees perform a type of “microbial farming” by inoculating 
pollen with specific microorganisms as they collect it and make it into a suitable mass to carry back 
to the colony. For example, Torulopsis magnoliae, a yeast, was added to pollen by the bees as were 
several Bacillus spp. and the molds Rhizopus nigricans (= R. stolonifer), Aureobasidium pullulans, 
Penicillium corylophilum, and P. crustosum. Bacillus spp. are exploited industrially for their 
production of numerous antibiotics, fatty acids which are also antimicrobial, and enzymes. Unlike 
Gram-negative bacteria, they secrete their chemical products extracellularly in large quantities. The 
conversion of pollen to bee bread has been postulated to be a microbial process similar to that which 
occurs in the fermentation of green food materials stored in silos. Thus, Bacillus spp., yeasts, and 
molds may stabilize stored pollen just as they do silage on its removal from the silo. 


The stored food of other social and solitary bees that were examined contain Bacillus spp., 
exclusively or predominantly, or no microbes. Also, there are similarities in the species of Bacillus 
associated with food of different origins in the nests of diverse bee species from various geographical 
areas (Gilliam et al. 1990a). Thus, a special association between Bacillus spp. and some bees may 
have evolved by which female bees inoculate food sources with these bacteria whose chemical 
products are responsible for the pre-digestion, metabolic conversion, fermentation, and preservation 
of food. 


Gilliam and Argauer developed and used a sensitive reproducible fluorometric method for analyzing 
Terramycin (TM; oxytetracycline hydrochloride) in bees, medicated diets, and honey (Argauer and 
Gilliam 1974; Gilliam and Argauer 1975, 1981; Gilliam et al. 1979). TM is the antibiotic that is used 
to control the bacterial diseases AFB and European foulbrood (EFB). Previously, TM had been 
analyzed by laborious microbiological methods which often did not yield quantitative data and were 
hampered by the presence of naturally occurring antibacterial substances in bees and their products. 
The stability of TM in various diet formulations fed to bees for disease control, the times and 
temperatures at which the diets can be stored, and degradation of TM in the hive were determined. 
Because honey for human consumption must not contain residues, TM was also analyzed in honey 
after feeding various medicated diets to bees. Results showed that TM is extremely stable in 
antibiotic extender patties, pollen patties, and sugar dusts, but degrades rapidly in sugar solutions. 
TM does not present residue problems if sufficient time (4-6 weeks) is allowed between the last 
treatment and extraction of surplus honey regardless of the method used to treat the bees. No residues 
were found in honey from colonies fed antibiotic extender patties. 


Gilliam and Taber (1973) and Prest et al. (1974) defined diseases and anomalies of honey bees in 
continuous bee production and in bees receiving artificial diets and massive amounts of pollen. This 
was one of the first published reports of chalkbrood disease, caused by the heterothallic fungus 
Ascosphaera apis, occurring in honey bees in the U.S. These studies also demonstrated that feeding 
massive amounts of pollen to rear all castes of honey bees throughout the year or feeding artificial 
diets to bees predisposes larvae and pupae to infections with fungi and adult bees to the disease 
caused by the protozoan Nosema apis. Taber and Lee (1973) reported that bee colonies in Arizona 
had peak infections of N. apis in the winter, but the disease virtually disappeared by late summer. 


Gilliam and Dunham (1978) isolated Bacillus pulvifaciens from dead larvae of honey bees from 
Arizona and Iowa. This organism is associated with powdery scale, a rare disease. They found that 


"scales" (dried remains of dead larvae) that have different appearances and colors can contain the 
organism. 


274 


As chalkbrood continued to spread throughout North America and to cause serious problems in some 
locations, Gilliam devoted more effort to research on the disease. Larvae with chalkbrood become 
mummified. There had been speculation that A. apis was not a primary pathogen but was a 
saprophyte growing on larvae dead from other causes. Gilliam et al. (1978) found that eggs and 
pupae did not support the growth of A. apis, but larvae of all ages and pre-pupae were susceptible. 
Infection occurred both through ingestion of A. apis and by the growth of the fungus through the 
cuticle. The fungus grew on larvae dead from other causes, but as a saprophyte, A. apis did not 
produce “mummies”. Variation in susceptibility of bee colonies was noted as an important factor in 
expression of the disease. 


Gilliam (1986) then demonstrated the wide range of susceptibility of individual bee colonies to the 
same dose of inoculum, elucidated various stresses which can trigger expression of the disease, and 
defined the substrates in the colony which can serve as sources of reinfection when the proper stress 
conditions exist. 


In other work, mating tests of separated strains of A. apis from chalkbrood mummies from various 
parts of the world demonstrated that all contained A. apis and that the pathogen in the U.S. does not 
differ from the one found elsewhere as had been suggested (Christensen and Gilliam 1983). 


Gilliam et al. (1983a) showed that genetically-controlled hygienic behavior of worker honey bees 
aids in control of chalkbrood by increased uncapping and removal of diseased and dead larvae 
(mummies) and by increased removal or decreased survival of the pathogen in bees and hive 
products. Beekeepers can use simple techniques devised to test the hygienic behavior of their bees 
(Gilliam et al. 1983b). Queens whose progeny exhibits poor hygienic behavior should be replaced. 
This work demonstrated that bees could be bred for resistance to chalkbrood disease and is important 
since no effective chemical control agent has been found. 


More recent work described improved, easier methods for testing hygienic behavior of bees (Gilliam 
et al. 1988; Taber and Gilliam 1988, 1989), showed that bee bread and guts of nurse bees were the 
major sources of the chalkbrood in susceptible colonies (Gilliam et al. 1988), and examined the role 
of normal microflora of bees and hive substrates in resistance of bee colonies to the disease (Gilliam 
et al. 1988). No antimycotic chemicals were produced by bees, brood, or hive substrates per se. 
However, microorganisms isolated from these sources were found to inhibit the growth of the 
pathogen. Most of these organisms were molds isolated from bee bread which were apparently 
introduced by the bees, as the pollen fed to the bees was remarkably free of microbes other than the 
pathogen. These results indicated that inhibitory molds, or their antimycotic products, which are part 
of the normal microflora of bee colonies, could be a control for the disease and that molds isolated 
from bee bread may play a role in resistance to the disease. 


The honey bee chalkbrood pathogen was isolated from diseased larvae of a carpenter bee, Xylocopa 
californica arizonensis, in Arizona and from the Asian honey bee, Apis cerana, from Korea. 
Ascosphaera apis strains from both bee species mated with A. apis strains from western U.S. honey 
bees and are thus interfertile and identical (Gilliam 1990). 


Because of recent interest in microbial control of ants, Gilliam et al. (1990b) reported on fungi 
isolated from a diseased queen rough harvester ant. Of the four molds isolated, either A/ternaria 
alternata (as tenuis) or Aspergillus flavus var. columnaris appeared to be responsible for the 
mycosis. All of the fungi isolated were provided to other researchers for testing on fire ants. 


Gilliam and Taber (1991) surveyed feral honey bee colonies for diseases, pests, and normal 


microflora and found only a few spores of N. apis and larvae of the greater wax moth. Honey bees 
from these colonies in central Arizona contained the same kinds of intestinal microorganisms as bees 


ZI0 


from managed colonies in southern Arizona. There were similarities in the kinds of microorganisms 
in bees and wax moth frass from feral colonies. They concluded that diseases were rare in these feral 
colonies, 28 of which had been observed for over five years. 


HORTICULTURAL CROPS RESEARCH LABORATORY, FRESNO, CA. By Patrick V. Vail, 
James E. Lindegren, and Darlene F. Hoffman 


Insect pathology research at the Stored Product Insects Research Laboratory (now a part of the 
Horticultural Crops Research Laboratory), Fresno, CA, began in 1966 with the hiring of W.R. 
Kellen, a graduate of the University of California, Berkeley. Much of Kellen's earlier work 
(University of California, Berkeley and California State Department of Public Health, Bureau of 
Vector Control, Fresno) involved studying the effects of pathogens on mosquitoes. Some of his 
cooperative work with ARS personnel included host-parasite interrelationships with 7. helohania from 
mosquitoes (Kellen et al. 1965, 1966). As an ARS scientist he conducted many studies on the 
ultrastructure, taxonomy, basic pathology and modes of transmission of protozoans that infected such 
insects as navel orangeworm, Indianmeal moth, and a number of coleopteran pests (Kellen and 
Lindegren 1968, 1971). Descriptions of these life stages have been valuable aids for identifying 
pathogens which are potential contaminants in established cultures. They also provide some 
indication of the potential of these organisms as microbial control agents. 


The symptomatologies of some of these protozoans were quite unique and Kellen's studies provided 
methods of simple and accurate diagnoses for these infections. For example, a protozoan isolated 
from the navel orangeworm caused melanized encapsulations which were clearly visible beneath the 
integument (Kellen et al. 1977a). These melanized spots were useful in diagnosis of advanced cases 
of infection caused by this pathogen. 


Kellen was the first to conduct studies on the use of Bacillus thuringiensis for the field control of the 
navel orangeworm in almonds (Kellen et al. 1977b). His results showed that proper timing of 
applications plus adequate volume and coverage were prerequisites for control of this insect. Results 
also pointed out the need for understanding adult and larval behavior in order to time applications for 
most effective control. The levels of control obtained indicated that the bacterial insecticide might be 
useful in an integrated pest management program. However, B. thuringiensis, up to the present time, 
has not been used commercially for the control of the navel orangeworm. With the increasing 
environmental and consumer concerns, the use of this pathogen may become more advantageous. 


Kellen directed a study on the symbiotic relationships of a Wolbachia that occurs naturally in the 
reproductive organs of the almond moth, a cosmopolitan pest of stored products (Kellen et al. 1981). 
The microorganism occurs in both males and females, but is transovarially inherited only through the 
cytoplasm of the egg. Although male moths do not transmit the symbiont, the presence of Wolbachia 
in the male causes the sperm to be “conditioned” so that such sperm is only accepted by an oocyte 
that contains a similar strain of Wolbachia. Therefore populations of moths that harbor different 
strains of symbionts are not interfertile. Kellen conducted intensive ultrastructural studies of the 
symbiont and also showed the relationships between symbiotic and aposymbiotic strains of the moth. 
This was the first time that this relationship was described from a lepidopteran. Kellen et al. (1972) 
also conducted a pioneering study on Rickettsiella from navel orangeworm. 


Kellen also conducted studies to elucidate the ultrastructure, pathogenicity and host specificity of 
two previously unknown small RNA viruses from larvae of the navel orangeworm, a serious pest of 
tree nuts in California. This investigation led to the discovery of the first known occurrence of a 
calicivirus in an invertebrate host (Kellen and Hoffmann 1981; Hillman et al. 1982). The 
ultrastructure of this virus was described by Hoffmann and Kellen (1982). Hillman et al. (1982) 
demonstrated two forms of the virus probably caused by partial degradation in the host's excreta and 


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compared their respective pathogenicities (Hoffmann and Hillman 1984). A picornavirus was also 
isolated and its pathogenic influence was described in the blood cells which are the primary tissue 
infected. These studies helped to focus attention on the small viruses of insects especially those 
species for which non-occluded viruses are unknown. Kellen conducted further studies on the small 
calicivirus, particularly on dose-mortality and the retarded growth responses of larvae (Kellen and 
Hoffmann 1982). No previous comparable studies with small non-occluded viruses had been 
conducted up to this time. Kellen found that stunted larvae usually succumbed to infection after an 
extended period in a moribund state during which they cease feeding, thus the term chronic stunt 
virus for this organism (Kellen and Hoffmann 1982). His research data indicated strongly that the 
virus was a suitable candidate as a biological control agent particularly from the standpoint of 
population management as opposed to a direct control procedure. 


The thermal stability of the calicivirus declined rapidly at temperatures of 55°C for 45 minutes or 
less. Also lower temperatures inactivated the virus but at a much slower rate. Of interest was the fact 
that larvae reared at 34°C, even though infected, showed a strong resistance to disease progression. 
Kellen proposed that high temperature rendered the insect unsuitable for infection because the 
enzyme systems required for the replication of the virus in vitro were inhibited by the temperatures 
(Kellen and Hoffmann 1983a). He also concluded that these studies pointed to the importance of 
understanding the microclimatic conditions that exist in the host-ecological niche. 


Kellen further studied the RNA viruses as related to the reduced longevity and fecundity of infected 
insects (Kellen and Hoffmann 1983b). His data showed that healthy moths lived about 15 times 
longer than their infected counterparts. Infected female moths laid 5- to 10-fold fewer eggs than their 
healthy counterparts. Moreover, healthy females mated with diseased males laid significantly fewer 
fertile eggs. These results showed the virus has subtle effects that could have significant impacts on 
host populations. Further studies may demonstrate inoculative releases of this virus are worthy of 
consideration as a pest management tool. 


In concert with the above studies, Kellen initiated investigations to elucidate the role of male 
Indianmeal moths (IMM) in the autodissemination of viral pathogens. By using females as an 
attractant, Kellen lured male IMMs to a dust formulation of IMM granulosis virus which then 
contaminated the males. Contaminated males in turn mechanically spread the virus to the body 
surfaces of the female moth, especially in the genital areas during the act of copulation (Kellen and 
Hoffmann 1987). Spread of a disease agent through mating is an efficient way of infecting 
individuals in a population. Kellen retired in 1986. 


In 1966, J.E. Lindegren began research at the Fresno location as an assistant entomologist. In his 
earlier studies, Lindegren, working with Kellen, discovered and helped to describe Nosema plodiae, 
a protozoan infectious to the IMM (Kellen and Lindegren 1968, 1971, 1973a, 1974b). Kellen's and 
Lindegren's early studies provided a point of reference for research on other undescribed 
microsporidans of stored product insect pests (Kellen and Lindegren 1969, 1970, 1972). 


Later in his investigations of the protozoa, Lindegren isolated a rarely reported pathogen of nitidulid 
beetles, propagated it for the first time under laboratory conditions, and investigated its host range 
and life cycle. As a result of electron microscope studies, he observed unreported stages of this 
pathogen's life history in the navel orangeworm (Lindegren and Hoffmann 1976). In further studies 
he extended its host range to include 15 species of insects in six families in three orders, and three 
species of mites (Kellen and Lindegren 1973b, 1974a). This work stimulated further investigations 
into the biological control potential of this pathogen (Fukuda et al. 1976) and studies of its life cycle. 


In the late 1970s, Lindegren began investigations on the control potential of entomopathogenic 
nematodes, primarily Steinernema carpocapsae. Early on, he found reasonably easy methods to 


oat 


produce the nematode (Lindegren et al. 1979b; Hara et al. 1981) and tested it under field conditions 
(Lindegren et al. 1979a, 1981a and b; Poinar et al. 1981). With $10,000 funding each from both the 
University of California and USDA-CSRS Interregional Project 4 (IR-4; clearance of pest control 
materials for minor use) for evaluation of carpenterworm control in fig orchards, Lindegren and 
associates developed the first commercial use of an insect parasitic nematode in the U.S. This 
technology was transferred to biosis®, Inc. An Environmental Protection Agency (EPA) exemption 
from tolerance for entomopathogenic nematodes was obtained which stimulated commercialization 
of nematodes for insect pest control. 


Lindegren's work on wood borers has been successfully used in the People's Republic of China, 
where it reportedly has saved highly valued shade trees. In addition, he demonstrated a broader host 
range of the nematode than was originally believed (Kaya and Lindegren 1983; Toba et al. 1983; 
Shapiro et al. 1985a; Lindegren 1990; Lindegren et al. 1992). One of his first field studies on the use 
of the nematode for control of the Colorado potato beetle was conducted in cooperative studies with 
the ARS Yakima Agricultural Research Laboratory (Toba et al. 1983). Initially dose-response curves 
were developed for this insect in the laboratory and again under field conditions. The studies showed 
that soil applications of entomopathogenic nematodes may be feasible as part of an integrated pest 
management program (Toba et al. 1983). These studies were later confirmed by industry and it is 
considered to be a safe and effective alternative for chemical insecticides used for Colorado potato 
beetle control. 


Other early investigations included determining the efficacy of nematodes for navel orangeworm in 
almond orchards (Lindegren et al. 1978, 1981b). Nematode field persistence, dose response, optimal 
application timing and effectiveness when applied with commercial sprayers (both ground and air) 
were determined in cooperation with the University of California Cooperative Extension Service and 
the almond industry (Agudelo-Silva et al. 1987; Lindegren et al. 1987). At a later date this control 
methodology was turned over to industries interested in producing the nematode and to the U.C. 
Cooperative Extension Service for commercial evaluation. Ancillary studies showed honey bees were 
only slightly susceptible to S. carpocapsae (Kaya et al. 1982). 


In cooperative tests in 1982 with the ARS Tropical Fruit and Vegetable Research Laboratory, 
Honolulu, HI, Lindegren conducted laboratory and field investigations which resulted in a nematode 
larvacidal soil drench for the reduction of Mediterranean fruit fly, oriental fruit fly, and melon fly 
populations (Lindegren and Vail 1986). Field evaluations of this entomophagous nematode as a soil 
treatment on Oahu and Maui in 1983, 1984 and 1985 indicated that the optimal concentration for 
control of "medfly" larvae when applied as a drench was approximately 500 nematodes per cm? 
(Lindegren 1990, Lindegren et al. 1990). Interest in this augmentative control method for fruit flies 
has been expressed by governmental agencies and industry (Lindegren 1992). 


Lindegren, with other scientists at the Horticultural Crops Research Laboratory, developed a 
technique for measuring the respiration rates of Steinernema feltiae infective juveniles to obtain 
information for optimum storage conditions (Lindegren et al. 1986). As a result of these studies, 
Lindegren developed a method of reducing respiration and increasing storage life of 
entomopathogenic nematodes by osmotic desiccation (Popiel et al. 1987). He also found desiccated 
nematodes could be stored in a viable condition at sub-zero temperatures. This method provided a 


means of long-term mass storage and shipment of steinernematid and heterorhabditid infective 
juveniles. 


Lindegren developed a simple, state of the art, in vivo rearing procedure for S. carpocapsae which 
produces only the infective juvenile stages. The method does not require the use of incubators, 
autoclaves or toxic disinfectants; provides an aerobic high relative humidity environment; screens 
against unwanted contaminants; and produces adequate nematodes for laboratory and small-scale 


278 


field tests (Lindegren et al. 1993). This method is currently being successfully used by private 
industry and other research facilities. In the late 1980s, Lindegren developed a process for storing 
entomopathogenic nematodes in a concentrated nematode-produced sponge-like mat or “nematode 
wool”. 


Lindegren also developed a selection method for increasing entomopathogenic nematode virulence, 
infectivity and production efficiency. As a result, the Kapow strain of S. carpocapsae produces 34% 
more infective juveniles six days earlier than the same unselected strain. The strain is also visibly 
more active, and at 50 nematodes per greater wax moth host larvae, exposures result in a three-hour 
earlier LT., than non-selected strains. The Kapow selection is being produced commercially. 


Lindegren is currently (1993) conducting cooperative studies (with the Western Cotton Research 
Laboratory, Phoenix, AZ) evaluating the control potential of pink bollworm with entomopathogenic 
nematodes (Lindegren et al. 1992). This approach looks promising and is stimulating the interest of 
industry. 


D.K. Hunter joined the insect pathology research group at the Stored Product Insects Research 
Laboratory soon after his 1967 graduation from the University of California at Riverside. Hunter 
conducted research almost exclusively on entomopathogenic viruses of stored product pests infesting 
dried fruits and nuts. His investigations included cytological and ultrastructural studies, virus-host 
interactions and the development of the viruses as microbial control agents. In 1970, Hunter reported 
on a granulosis virus (GV) first isolated from the almond moth infesting stored peanuts from Georgia 
(Hunter and Dexel 1970). Electron microscope studies indicated a pathology similar to that reported 
for the Indianmeal moth GV (Hunter and Hoffmann 1970). Similar studies on pathogenicity were 
conducted by Hunter on the Indianmeal moth GV (Hunter 1970; Hunter et al. 1972; Hunter and 
Hoffmann 1973). Cross-infectivity tests showed that the Indianmeal moth GV failed to infect first 
instar larvae of tobacco, almond, and raisin moths, at concentrations much higher than the LD,, of 
Indianmeal moth. Hunter determined the influence of high temperature on respiration and mortality 
of Indianmeal moth exposed to other GVs (Hunter and Hartsell 1971). Larvae exposed to the virus 
had a lower respiration rate than healthy larvae. In a temperature mortality test, the highest mortality 
occurred at 32°C. Treated larvae at 37°C did not display granulosis symptoms, but they apparently 
harbored the virus. He noted that control larvae at 37°C were less developed, greenish and generally 
less healthy appearing than larvae reared at lower temperatures. These studies suggested that the 
infection was masked or thermally inhibited at high temperatures. Interestingly, larvae at 32°C were 
the first to die with granulosis. To evaluate the efficacy of direct applications of the Indianmeal moth 
GV to commodities prior to storage, virus suspended in water was sprayed on conveyor-borne 
almonds, peanuts, walnuts and raisins. These were then infested with Indianmeal moth eggs and held 
in simulated storage conditions. In every case, the virus treatment protected the commodity 
effectively (Hunter et al. 1973, 1975, 1977, 1979). 


Because of the specificity of the virus, an investigation of its compatibility with malathion was 
conducted so that in combined applications beetles that are also storage pests would be controlled 
along with the Indianmeal moth which had become resistant to malathion. Results showed that the 
mixture of granulosis virus and malathion was more effective against the Indianmeal moth than either 
material alone. At the same time, the test beetles were significantly controlled (Hunter et al. 1975). 


In 1978, P.V. Vail was transferred to the Horticultural Crops Research Laboratory to conduct 
investigations on the basic pathology and microbial control of pre- and postharvest pests. In a series 
of studies, he demonstrated that ACMNPV was 10 times more infectious to tobacco budworm than to 
corn earworm, important pests of cotton and other crops (Vail et al. 1978). These studies pointed to 
the importance of knowing which species of the Heliothis/Helicoverpa complex was infesting a crop 
(Vail et al. 1978). Further studies with AcMNPV and Helicoverpa zea and Heliothis virescens 


219 


showed that virus replication and inclusion body production were much lower in the corn earworm 
whether the inoculum was administered per os or by injection into the hemocoel (Vail et al. 1982). 
Non-occluded virus (NOV) production in six tissues of corn earworm was significantly reduced as 
compared to tobacco budworm (Vail and Vail 1987). The above studies provided a pathological basis 
for research conducted by Vail and Max Summers of Texas A&M University on the infectivity of 
AcMNPV-like baculovirus isolates, variants and recombinants. These viruses were no more potent 
than the wild type AcMNPV for corn earworm or tobacco budworm and it was concluded that the 
known viruses of the ACMNPV type probably do not have the phenotypic variability needed for 
increased infectivity to corn earworm (Vail et al. 1982). Furthermore, passage of wild-type AcMNPV 
through corn earworm did not increase its virulence, although three new variants were isolated. 
Therefore, other sources must be found, either natural, selected or engineered, of ACMNPV-type 
baculoviruses having more activity towards corn earworm. In 1985, such a virus was isolated near 
Columbia, MO, from the celery looper, with a broad host range and high activity towards both H. zea 
and H. virescens. The virus was patented by ARS. Field tests were initiated in 1990 to determine the 
potential of this virus as a microbial control agent (Vail et al. 1992). 


Together with T.J. Morris of the Department of Plant Pathology, University of California, Berkeley, 
Vail conducted research on a calici-like virus (Trichoplusia ni RNA virus [TRV]) isolated as a 
contaminant of an AcMNPV preparation (Morris et al. 1981; Vail et al. 1983a). Vail and Morris 
found several noncontaminated preparations and traced the lineage of contaminated preparations. 
Quality control procedures were developed that would preclude contamination (Vail et al. 1983b). 


Vail and associates found that a granulosis virus of the IMM could be produced much more cheaply 
and could provide excellent and cost effective protection (up to 100%) of dried fruits and nuts from 
this insect through the normal life of these commodities in marketing channels. Damage could be 
reduced to the point where an infestation would be of no economic consequence (Cowan et al. 1986). 
Further studies showed the virus will provide control for the time these commodities will remain in 
the marketing channels. Further developments of the formulation and production have led to a 10- 
fold reduction in cost and made the virus economically competitive with both presently used 
fumigants and newly developed controlled-atmosphere methods of control (Vail et al. 1991). This 
research was important because it provided a control method to the dried fruit and nut industries in a 
“niche” (e.g., marketing channels) which did not previously exist. 


Studies were conducted to further elucidate the role of digestive juices in the susceptibility of various 
insects to ACMNPV (Elam et al. 1990). By extraction of the gut juices of species with low and high 
susceptibility and subjecting polyhedra to these fluids it was determined that the digestive fluids 
were not a barrier to infection. They also found that infectivity patterns were different when 
polyhedra were dissolved in sodium carbonate solutions or digestive fluids suggesting different 
modes of dissolution (Elam et al. 1990). 


In the early 1980s, the laboratory was approached by R.E. Teakle of Australia concerning the export 
of the AcMNPV for testing on Australian Heliothis/Helicoverpa species. However, the virus could 
not be exported because of the concern of Australian quarantine officials that the virus might infect 
Cactoblastis cactorum, an important biological control agent of pricklypear cactus. Therefore, C. 
cactorum was imported to the Fresno laboratory and, based on bioassays, histological and restriction 
endonuclease studies of the virus versus C. cactorum, it was concluded that the insect was 
moderately susceptible (Vail et al. 1984). These results showed that caution should be used when 


introducing a new pathogen into an area where biological control organisms of related target hosts 
may exist. 


An Insect Affecting Man and Animals Laboratory was located in Fresno from 1968 to 1977. 
Investigations of this laboratory were primarily involved with the blood-sucking Diptera. T.B. Clark 


280 


was hired in 1973. His research emphasis was on finding and identifying pathogens of these insects. 
He was one of the first investigators to conduct research on the impact of Beauveria bassiana on a 
number of mosquito species (Clark et al. 1968). Clark and O'Grady (1975) described a non-occluded 
virus from Culicoides cavaticus. Mortality rates ranged from 70 to 90% in field-collected larvae. 
Virus-like particles were observed in the epidermal cells, in and on the surface of muscle bundles, in 
gut cells and in the tracheal epithelium. Although similar in signs and symptoms to pathogens of 
Culex tarsalis and C. salinarius, attempts to cross transmit the pathogen to these and several other 
species were unsuccessful. 


Clark also conducted investigations on a Tetrahymenine ciliate isolated from Aedes sierrensis in 
Fresno County, California (Clark and Brandl 1976). Melanized black spots on the cuticle were found 
associated with sites of invasion or attempted invasion by this organism. Successful invasion of the 
ciliate into the host occurred within 20 hours after exposure. Interestingly, cysts on the integument 
were lost during the molt and cast off with the exuviae during molting. As of 1976, the taxonomic 
status of this ciliate remained in question. Clark transferred to Lake Charles, LA, in 1974 and 
eventually became a staff member at the ARS Insect Pathology Laboratory in Beltsville, MD, where 
he conducted research on honey bees. 


BOYDEN ENTOMOLOGICAL LABORATORY, RIVERSIDE, CA. By Patrick V. Vail and 
David K. Reed 


An insect pathology/microbial control program was begun in the early 1960s at the USDA-ARS 
Boyden Entomological Laboratory on campus at the University of California at Riverside. At that 
time two research entomologists began research on the classical cabbage looper, singly-embedded 
nuclear polyhedrosis virus which is known by the present nomenclature as TnSNPV. The first ARS 
experiments with this virus were conducted by J.C. Elmore in the late 1950s while still at Whittier, 
CA. In 1961 he published a paper on the control of the cabbage looper with this NPV (Elmore 1961). 
His promising results led to further tests by him and A.F. Howland. Instead of spraying the virus on 
plants as in the previous studies, Elmore and Howland investigated the possibility of artificially 
contaminating moths and thus disseminating the NPV to their progeny (Elmore and Howland 1964). 
They found that a maximum of 51% of the progeny from moths sprayed with a virus suspension were 
diseased. However, in the same set of tests they found the application of the virus by spray onto the 
foliage was more effective than dissemination by the moths. This work conducted in the early 1960s 
was a precursor of a pathology program that was in existence at the Boyden Laboratory until 1969. 


In 1962, P.V. Vail assumed an appointment at the Boyden Laboratory and one year later began 
conducting research on various entomopathogenic viruses infectious to vegetable insects. These 
studies were both basic and applied in nature with the eventual goal of being able to understand and 
utilize these pathogens as control agents for vegetable insects. In the early days of semi-artificial diet 
laboratory assays of entomogenous viruses, formalin was a commonly used component in the diets to 
preclude or prevent microbial contamination and growth. However, formalin also was known to be 
an antiviral agent and Vail showed that formaldehyde, even at very low concentrations in the diet, 
caused inactivation and reduction of apparent activity in bioassays (Vail et al. 1968). 


In attempts to find out more about the epizootiology and transmission of nuclear polyhedrosis viruses 
as they were used in the studies conducted by Elmore and Howland (1964), Vail conducted intensive 
basic research on the influence of the cabbage looper SNPV on the postlarval stages of the cabbage 
looper with attention to transmission of the virus to progeny. He found that, for the most part, adults 
emerging from pupae that were infected as larvae transmitted very little virus to their progeny either 
on or in the egg (Vail and Hall 1969b and c; Vail and Gough 1970a). However, pupae and adults 
could be infected by inoculation into the hemocoel. Vail investigated transmission by moths 
emerging from inoculated pupae and by moths that had been inoculated as adults and found that the 


281 


levels of transmission also were quite low. All of the transmission that did occur was on the surface 
of the egg or by contamination by the meconium or feces from the adult moths. No significant 
transmission of the viruses occurred in the egg even though the reproductive tissues of both sexes 
were found to be infected. Interestingly, pigmentation of many moths emerging from inoculated 
pupae was reduced significantly. Intensive histological studies were conducted (Vail and Hall 
1969a). 


In 1967, Vail isolated a cytoplasmic polyhedrosis virus from the cabbage looper which was found to 
have manifold effects on larval development, pupal and adult size, and adult deformities. He studied 
this virus intensively to measure the effects on reproduction as related to the size of emerging 
infected adults. Because of reduced size due to infection, reproduction of adults was significantly 
reduced. Although transmission of this virus also occurred on the egg, transmission of the virus 
within the egg was not demonstrated (Vail et al. 1967, 1970; Vail and Gough 1970a and b). 


While at the Boyden Laboratory, Vail also conducted numerous field tests with entomogenous 
viruses (Vail et al. 1971c). These tests showed that both the nuclear and cytoplasmic polyhedrosis 
viruses could reduce cabbage looper populations when applied alone or in combination. The degree 
of control compared favorably with that obtained with chemical insecticides. 


In 1967, Vail isolated a multiply-embedded nuclear polyhedrosis virus from a single larva of the 
alfalfa looper and proceeded to conduct in-depth studies on this virus (AcMNPV) in which virions 
were occluded multiply in the polyhedral matrix. At first it was found that both the classical TnSNPV 
and AcMNPV were reciprocally infective to both the alfalfa looper and the cabbage looper (Vail 

et al. 1971b). Later studies showed that AcMMNPV had a much broader host range than any previously 
described insect virus. Because of this, host-range studies were conducted on other species of 
Lepidoptera including the beet armyworm and Heliothis/Helicoverpa spp. (Vail et al. 1971a, b and c; 
Vail and Jay 1973). 


Vail conducted intensive basic studies on ACMNPV including the histopathology and relative 
infectivity and also conducted tests with this virus in the field. Because of its broad host range, this 
virus changed the classical views concerning the specificity of nuclear polyhedrosis viruses. This 
virus has been studied by many investigators using in vitro and in vivo techniques. It was the first 
NPV found to replicate extensively and completely in an insect cell line (Vail et al. 1973b). 
Infectivity of polyhedra following one passage was normal. The host range of this virus is now 
known to include many species in numerous families of insects including many economically 
important species to agriculture and forestry worldwide. 


In 1969, the pathology program at the Boyden Laboratory was terminated upon the move of Vail to 
the Western Vegetable and Sugarbeet Investigations Laboratory, Mesa, AZ. Later, after moving to 
Phoenix, AZ, Vail completed further studies on ACMNPV for control of cotton and vegetable insects 
(see above). Now this virus is also prominently used in the field of medicine and biology for the 
production of biologically active compounds such as vaccines, proteins needed for immunology and 
complex therapeutic compounds. 


Although reports of mite viruses are not common in the literature, one such virus was intensively 
researched by scientists at the Boyden Laboratory. This non-occluded virus attacks the citrus red mite 
exclusively (Shaw et al. 1967; Beavers and Reed 1972), and has potential for use in mite 
management programs. Extensive basic and applied research was conducted on this virus of the 
citrus red mite over a period of about 14 years by a number of scientists, principally D.K. Reed. The 
etiological agent was first characterized by Smith et al. (1959) as a spherical particle, 35 nm in 
diameter, but later identified by Reed and Hall (1972) and Reed and Desjardins (1982), as rod- 
shaped, 58 x 194 nm, and enclosed in envelopes, 111 <x 266 nm. Such rods form in the nuclei of 


282 


midgut epithelial cells and generally acquire an envelope, composed of single or multiple layers, as 
they pass through the nuclear membrane. The spherical particles reported by Smith et al. (1959) are 
present in healthy, as well as in diseased mites (Reed and Desjardins 1978), being composed of three 
sizes, 18 nm in crystalline array, and 30 and 37 nm particles. The virus is apparently transmitted from 
mite to mite by contact with viral particles within feces and debris on the plant surface deposited by 
infected mites (Reed et al. 1975). The “suction cup” feeding mechanism of these mites (Jeppson et 
al. 1975), along with the abundance of virus rods within the hindgut cells being continually sloughed 
into the gut lumen to be defecated, indicates a highly infectious fecal pellet. Envelopment of the 
virions in a matrix of cellular material may explain why natural infective material on contaminated 
surfaces lasts so much longer than aqueous sprays (Reed et al. 1975). Gilmore and Munger (1963) 
reported eight days while Tashiro et al. (1970) reported 28 days residual activity from contaminated 
surfaces of lemons. Aqueous sprays generally survive only 2-4 hours (Gilmore and Munger 1963), 
probably inactivated by ultraviolet radiation. Tashiro et al. (1970) reported viruses in intact mites 
retained viability >28 days in the laboratory and postulated that such intact dead bodies could adhere 
to plant surfaces as reservoirs. Shaw et al. (1972) found complete viability of virus in infected mite 
bodies after 6.5 years in storage at -5°C. Acaricide use in glasshouses had no effect on initiation of 
epizootics (Shaw and Pierce 1972). Shaw et al. (1969) obtained good control of mites in glasshouses 
where temperatures were moderate. Laboratory studies indicated that virus particles within mite 
bodies were unaffected by normal orchard temperatures (40.5°C), but activity was lost after 6 hours 
exposure at 46°C and | hour exposure at 60°C (Reed 1974). 


The formation of birefringent crystals within diseased mites makes identification simple and rapid 
(Smith and Cressman 1962). Reed et al. (1972c) related these crystals to normal production of fecal 
pellets, showed that high humidity inhibited such production (Reed et al. 1974), and developed a 
portable apparatus to detect such crystals in the field (Reed et al. 1972a). 


Collections of diseased mites for research in the field was facilitated by using vacuum-suction 
machines, saving 95—98% over the cost of laboratory rearing (Shaw et al. 1971), and increased 
infection of collected mites was expedited by holding them on green lemons (Reed et al. 1972b). 
Since aqueous applications are inadequate for control of mites in the field, Reed et al. (1973) tested 
spray additives and extenders and found that extracted body fluids from cabbage looper larvae and 
pupae extended activity for 144 hours in the laboratory, although field trials were inconclusive. 


The citrus red mite virus occurs naturally in mite populations throughout the citrus-growing areas of 
California and Arizona and exerts considerable natural control of large populations of mites (Tashiro 
and Beavers 1966; Shaw et al. 1968b). Although there now exists no economical or practical method 
of applying the virus (Shaw et al., 1968a) at opportune times, many growers and crop advisors 
recommend delaying acaricide applications in high mite densities to allow epizootics to become 
established. Hopefully, more research will be done in the future on practical usage of a viable 
management tool that has been, for the most part, neglected. 


MEDICAL AND VETERINARY ENTOMOLOGY RESEARCH LABORATORY, GAINESVILLE, 
FL. By Albert H. Undeen and Donald P. Jouvenaz 


One of the major long term objectives of the Insects Affecting Man and Animals Research 
Laboratory (currently named the Medical and Veterinary Entomology Research Laboratory) at 
Gainesville, FL, was mosquito control. This was, in large part, a response to the needs of the 
military. During the mid-1960s D.L. Bailey reported on some microsporida of mosquitoes (Bailey 
et al. 1967a and b) but a directed effort towards microbial control of mosquitoes really began at 
Gainesville with the work of E.I. Hazard (1963-81). The main goal was then, and remains, to find 
pathogens of mosquitoes that would exert continuous suppression on mosquito populations, without 
frequent reapplication. Although Hazard studied a wide variety of pathogens, his most important 


283 


work was with the microsporida. Working with J. Weiser in Czechoslovakia, he made the landmark 
discovery that “7helohania’”’ in larval and “Nosema” in adult mosquitoes were portions of life cycle 
stages of one species (Hazard and Weiser 1968). His taxonomic work on this group is summarized in 
a USDA-ARS Technical Bulletin (Hazard and Oldacre 1975) that is still in use for the identification 
of this large group of microsporida. Hazard also published detailed descriptions of their peculiar 
meiosis (Hazard et al. 1979; Hazard and Brookbank 1984). In the early 1970s, he also studied 
microsporida such as Nosema algerae, at that time under consideration for control of malaria vectors. 
After his transfer to Lake Charles, LA (see below), he continued working on microsporidan life 
cycles, describing the development and fusion of gametes of Amblyospora. Finally, working with 
A.W. Sweeney of Australia, the discovery was made that a copepod intermediate host was an 
essential part of the life cycle (Sweeney et al. 1985). The description of a third kind of spore in the 
copepod and its infectivity for mosquito larvae finally completed the life cycle of one of the 
commonest forms of microsporida in mosquitoes and other biting flies. 


R.E. Lowe (1966-72) examined the potential of Conidiobolus (as Entomophthora) coronata (Lowe 
et al. 1968; Lowe and Kennel 1972). With a series of graduate students, he examined the control 
potential of several mosquito viruses (Federici and Lowe 1972; Hall and Lowe 1971, 1972; Lowe 
et al. 1970; Matta and Lowe 1969, 1970). As a result of this research, the viruses, at least for the 
moment, have been removed from consideration for biological control of mosquitoes. 


K.E. Savage (1966-77) started as a technician and earned his M.S. degree with a thesis on the 
bionomics of N. algerae in 1966. He contributed interesting findings on transmission of malaria 


(Plasmodium gallinaceum) by mosquitoes concurrently infected with N. algerae (Savage et al. 1971). 


D.W. Anthony (1969-1979) also completed his M.S. degree while employed at the Gainesville 
laboratory and went on to develop procedures for electron microscopy studies on mosquito 
pathogens. Later, Anthony led a group that developed production and application methods for the use 
of N. algerae against anopheline mosquitoes, culminating in a field trial in Panama (Anthony et al. 
1978a and b). 


S.W. White (Avery) has worked on WN. algerae at the Gainesville location since 1975. Her 
contributions have been in all areas of pathology and biological control. A major contribution was 
the description of the early stages of NV. algerae development in mosquito larvae by electron 
microscopy (Avery and Anthony 1983). Research on the biology and biological control potential of 
anopheline pathogens (Avery and Undeen 1987b, 1990) and methodologies for pathogen surveys 
(Avery and Undeen 1987a) have been her long-term responsibility. She also brought the laboratory 
into the computer age. 


Anthony retired in 1979, to be replaced a year later by A.H. Undeen (1980-present). While 
continuing work begun in Newfoundland on the control of simuliid larvae in small streams with 
Bacillus thuringiensis israelensis (Bti) he initiated research on microsporidan spores, concentrating 
on how they accomplished their seemingly explosive germination. Findings were summarized in a 
paper on the biophysical-biochemical basis of the germination process (Undeen 1990). He has used 
this knowledge of spore germination in work with the grasshopper biological control agent, Nosema 
locustae (Undeen and Epsky 1990), and in an effort to improve the storage time of Edhazardia aedis, 
a promising pathogen for container-inhabiting mosquitoes. 


L.A. Lacey (1981-86) and Undeen described the effects of formulation and treatment parameters on 
the efficacy of Bti against black flies under natural conditions (Lacey and Undeen 1984) and 
developed a simplified method for dosage calculation in small streams (Undeen et al. 1984). Lacey 
went on to develop methods of application, and test a variety of formulations of Bti and B. 
sphaericus in many mosquito and black fly larval habitats. These bacterial products were shown to 
be useful additions to the larvicide arsenal. In the laboratory, Lacey developed testing protocols, and 


284 


explored new formulation ideas. The safety of Bacillus pathogens to non-target organisms was also 
investigated (Undeen and Lacey 1982; Lacey and Mulla 1990) and particularly on Toxorhynchites 
mosquitoes (Lacey and Dame 1982; Lacey 1983; Lacey and Harper 1986). Especially sought after 
was a formulation or isolate that would persist in the larval site for prolonged periods. Bacillus 
sphaericus partially met these requirements (Lacey et al. 1987). He investigated the long-term effects 
of B. sphaericus on the physiology and behavior of surviving mosquitoes (Lacey et al. 1987). Lacey 
left Gainesville in 1986 for a position with the U.S. Agency for International Development (AID). 


J.C. Lord (1987-90) succeeded Lacey in this line of work. He conducted intensive research on 
sustained release formulations of Bti and B. sphaericus and conducted a worldwide search for new 
and better isolates of the latter. His most important publications are in press (as of 1993). 


In 1985, after the closure of the Lake Charles, LA, Gulf Coast Mosquito Research Laboratory, J.J. 
Becnel, Tok Fukuda, Roy McLaughlin, and O.R. Willis were reassigned to Gainesville. Becnel 
completed his Ph.D. research at the University of Florida with a dissertation detailing the life cycle 
and biology of the polymorphic microsporida, based on research begun at Lake Charles with Hazard. 
He described the life cycles of microsporida in mosquitoes including Edhazardia aedis, a 
microsporidan isolated from Aedes aegypti in Thailand (Becnel et al. 1989). He is now (1993) 
evaluating its potential for control of container-inhabiting mosquitos. Fukuda took over the electron 
microscope facility and, with O.R. Willis, conducts searches for new pathogens. 


Over the years, graduate students have played an important role in the Gainesville research program. 
In the early 1970s, James Matta worked with viruses, as did Don Hall, now a professor at the 
University of Florida, and Brian Federici, presently a professor at the University of California, 
Riverside. Later, Steve Hembree, an Army entomologist, published numerous papers on viral 
pathogens of mosquitoes. John Kelley, John Knell, Frank Van Essen, and John Putnam all did their 
thesis work on microsporida of mosquitoes. 


The imported fire ants, Solenopsis richteri and S. invicta were introduced into the U.S. from South 
America ca. 1920 and 1940, respectively. By 1991, these medical and agricultural pests infested over 
10° hectares in 11 southeastern states and Puerto Rico (Lofgren 1986). Recently, isolated colonies 
were detected in Arizona and California. If they become established in the more humid or irrigated 
areas of the western U.S., their range will increase substantially. In addition, a polygynous form of S. 
invicta having denser populations is spreading within the population (Glancey et al. 1987). The ARS 
Imported Fire Ant project began in 1968. Its biological control component began in 1974. 
Conceptually, the primary goal was the permanent amelioration of the imported fire ant problem 
through the establishment of a complex of host-specific natural enemies. A secondary goal was the 
development of a microbial insecticide(s). 


As a Postdoctoral Fellow (1970-71) B.A. Federici, and later D.P. Jouvenaz of the Medical and 
Veterinary Entomology Research Laboratory and his colleagues, examined S. invicta from Florida 
and demonstrated that they were essentially free of host-specific natural enemies. In their native 
South American range, they are beset by pathogens, parasites, social parasites, and symbiotic 
predators. 


The first specific pathogen of fire ants was observed by W.F. Buren, a medical entomologist and 
myrmecologist, who retired from the U.S. Public Health Service in order to pursue fire ant 
systematics at the Medical and Veterinary Entomology Research Laboratory under a grant from 
ARS. In 1973, Buren noticed cyst-like bodies in the gasters of alcohol-preserved workers from Brazil 
which were identified by E.I]. Hazard as membrane-bound masses of microsporidan spores. With 
Hazard's guidance, J.D. Knell, a University of Florida Postdoctoral Fellow under G.E. Allen, 


285 


described the pathogen from fresh material, naming it Thelohania solenopsae (Knell et al. 1977). 
This pathogen proved to be ubiquitous in fire ants in South America. 


The discovery of a pathogen of fire ants stimulated interest in biological control research. In the 
summer of 1974, the first of a series of trips to Brazil was made to search for natural enemies of fire 
ants. The team members were Hazard, Jouvenaz, W.A. Banks, and D.P. Wojcik. M.A. Naves, a 
Brazilian doctoral student at the University of Florida, accompanied the team as guide and 
interpreter. On this and four subsequent trips, research was headquartered at the Universidade 
Federale de Mato Grosso, Caceres, under an agreement with the University of Florida, negotiated by 
G.E. Allen. 


Because of his interest and background in microbiology, pathology research was assigned to 
Jouvenaz; the arthropod symbionts became the province of Wojcik. Reasoning that the imported fire 
ants had escaped their specific natural enemies, Jouvenaz studied S. geminata, a fire ant known to be 
of Caribbean origin introduced into Florida long ago, as a model. Survey procedures for disease were 
developed and employed in an intensive survey in six states which confirmed the absence of disease 
in imported fire ants (Jouvenaz et al. 1977). The only microorganism found to be symbiotic with 
imported fire ants was a yeast-like fungus which was apparently only a nutritional burden (Jouvenaz 
and Kimbrough 19972). 


In contrast to the imported species, S. geminata hosts several species of parasitic protozoa (Jouvenaz 
1984), a rare mermithid nematode (Mitchell and Jouvenaz 1985), and a virus (Jouvenaz, 
unpublished). The microsporidan Burenella dimorpha Jouvenaz and Hazard (1978) was studied 
intensively as a model for basic pathobiology and development of techniques and became the subject 
of Jouvenaz's doctoral dissertation (1982). A review of this and other pathogens of fire ants may be 
found in Jouvenaz (1986). 


During the early pathogen surveys in Brazil, the first virus known from fire ants (the second known 
ant virus) (Avery et al. 1977) and an undescribed protozoan were collected by Banks and Jouvenaz. 
Additional data on ant populations and incidence of disease in them were collected (Jouvenaz et al. 
1980; Banks et al. 1985). From material collected abroad, Jouvenaz and Ellis (1986) described 
Vairimorpha invictae and its effects on the host. 


More recent searches in Brazil provided a nematode, Tetradonema solenopsis (Nickle and Jouvenaz 
1987). This parasite is able to invade adult queens and has the potential for eliminating established 
colonies. Taxonomic work has indicated that it is probably host-specific and, therefore, 
environmentally safe. Attempts to propagate a parasitized colony at the Medical and Veterinary 
Entomology Research Laboratory and at Caceres failed, due to rapid death of parasitized ants when 
subjected to stress. Valuable information on the arthropod symbionts of fire ants, such as their use of 
chemical mimicry to integrate into ant colonies (Vander Meer et al. 1989), was also gained. The 
observation of two non-pathogenic neogregarines (one of which appears identical to Mattesia 
geminata [Jouvenaz and Anthony 1979]) was of academic interest only. Attempts to study fire ant 
epizootiology and population dynamics in Brazil were frustrated by the extreme and prolonged dry 
season. On one occasion, however, fire ants had virtually disappeared from an area in which there 


was a very high population density with a high incidence of disease a few months earlier (Jouvenaz 
1990b). 


Under a new agreement with the Biological Control of Weeds Laboratory, USDA-ARS, in Argentina, 
Wojcik and Jouvenaz visited Argentina in October, 1987, to survey for natural enemies of fire ants. 
J.A. Briano joined the fire ant project and was trained at the Medical and Veterinary Entomology 
Research Laboratory; he subsequently completed course requirements for a M.S. degree at the 
University of Florida in 1991. In April 1988, Briano and Jouvenaz located acres in Argentina suitable 


286 


for monitoring disease and ant population dynamics. Under the direction of R.S. Patterson, who suc- 
ceeded C. Lofgren as Research Leader upon the latter's retirement, Briano began monitoring the 
impact of naturally occurring Thelohania solenopsae and Vairimorpha invictae on field populations 
of fire ants. 


Also during this period, two trips were made by Wojcik to collect fire ants for taxonomic study, 
zoogeographical records, and pathogen screening. In 1987, Wojcik and A. de Campos collected 
extensively in Brazil and in 1990, Wojcik, Patterson, and Briano sampled from a wide area including 
parts of Argentina and Uruguay. More than 1,000 samples were collected providing needed 
information on the distribution of Tetradonema solenopsis and other parasites. This work revealed 
that many pathogens known from Brazil were also found in Argentina, although the nematode 7. 
solenopsis appeared to be absent. A new but rare mermithid nematode of dubious biological control 
value was found; efforts to propagate it failed (Jouvenaz and Wojcik 1990). The obligate 
endoparasitic fungus, Myrmecomyces annellisaes, not seen in Brazil, was found in Argentina. 
Arthropod symbionts — possible intercolonial vectors of disease — were abundant. 


Susceptibility of fire ants to a wide variety of general entomopathogens, pathogens of other 
Hymenoptera, and even other orders was tested. Jouvenaz eventually demonstrated that typical 
entomopathogenic bacteria are not ingested, but are removed from food by pharyngeal filtration 
(Jouvenaz 1990a, 1991). Tests with commercially-produced steinernematid nematodes (biosys®, 
Inc., Palo Alto, CA) demonstrated that previous encouraging reports of control were a result of 
unrecognized nest relocation (Jouvenaz et al. 1990). Jouvenaz retired in 1991. Briano continued 
research on various aspects of fire ant biology and biological control in South America under the 
direction of Patterson. 


SUBTROPICAL INSECTS RESEARCH LABORATORY, ORLANDO, FL. By William J. 
Schroeder and Clayton W. McCoy 


An insect pathology program was initiated at the Subtropical Insects Research Laboratory, Orlando, 
FL, in 1966 with the hiring of C.W. McCoy. He was to conduct investigations on the microbial 
control of the citrus rust mite infesting Florida citrus. McCoy substantiated infection of the mite by 
the fungus Hirsutella thompsonii in the field, and also by infection of laboratory-reared mites with 
laboratory-produced spore material. McCoy and Kanavel (1969) then conducted research to 
determine the optimal solid media for culture of H. thompsonii. On several of the more productive 
media, maximum production (rates not absolute values) of conidia was obtained 12 days after 
inoculation. Growth was demonstrated to be dependent upon a number of nutritional factors in the 
complex media. McCoy et al. (1971) also showed that citrus rust mite could be suppressed with 
applications of fragmented mycelium. Therefore a liquid medium for the large-scale production of H. 
thompsonii in submerged culture was developed (McCoy et al. 1972). Aeration was essential for 
growth and sporulation did not occur in submerged culture. Later, mycelia obtained from submerged 
culture were formulated for applications in the field (McCoy et al. 1975). A review of the 
development of this fungus as a miticide was provided by McCoy and Selhime (1973). Later the 
fungus was produced commercially and registered by Abbott Laboratories. The product (Mycar®) 
was sold commercially until 1983; at this time it is not used commercially. 


Research on entomopathogenic nematodes began in 1980 when entomologists at the Laboratory 
conducted a survey of soil insect pathogens of the citrus root weevil complex (comprised of Fuller 
rose beetle, the "little leaf notcher" [Artipus floridanus], the citrus root weevils [Pachnaeus opalus 
and P. litus], and the "sugarcane rootstock borer weevil" [Diaprepes abbreviatus]) and isolated 
heterorhabditid and steinernematid nematodes (Beavers et al. 1983). Early research was conducted 
with biosys® and H.K. Kaya of the University of California, Davis. It was not until 1987 that 
publications (Schroeder 1987, 1990) were generated on the potential use of this biopesticide for 


287 


management of the citrus root weevil complex. In general, when weevil larvae were exposed to 
nematodes in the laboratory and in greenhouse tests the infection rate was 60%. By 1988, it was 
possible to produce enough nematodes to attempt a pilot program for weevil management. The 
Orlando laboratory received $30,000 per year for three years to provide for production and 
application of nematodes on a 10-acre block of citrus. A cone ground trap was used to evaluate adult 
emergence (Schroeder 1990). With this efficacy data, entomopathogenic nematodes were added to 
the 1991 Florida Spray Guide (Schroeder 1992). In 1991, 10,000 acres of citrus groves and nurseries 
were treated. The acreage increased to 20,000 in 1992 and 30,000 by 1993. 


INSECT BIOLOGY AND POPULATION MANAGEMENT RESEARCH LABORATORY, 
TIFTON, GA. By John J. Hamm 


The Southern Grain Insects Research Laboratory was established in Tifton, GA, in 1960. In 1984, the 
name of the laboratory was changed to the Insect Biology and Population Management Research 
Laboratory. The mission of the laboratory was to develop control methods for corn earworm and fall 
armyworm, the primary pests of grain in the Southeast. The position of Insect Pathologist was 
originally held by Paul Surany who set up the insect pathology laboratory at Tifton but soon left to 
go to the Forest Service. 


J.J. Hamm joined the staff at the end of 1962 to work on insect pathology and microbial control. This 
was a time when much research was being done on establishment and maintenance of insect colonies 
for potential use in mass production and release of sterile insects or for production of parasitoids. 
Part of the mission of the insect pathologist was to help maintain disease-free insects for mass 
production and research. 


Hamm (1968) compared a nuclear polyhedrosis virus (NPV) of fall armyworm to a granulosis virus 
(GV) of fall armyworm from South America, and determined that the NPV had more potential for 
biological control because of the faster kill. Young and Hamm (1966) combined corn earworm NPV 
and fall armyworm NPY to protect sweet corn from both insects. Hamm and Young (1971) 
demonstrated the importance of an early-tassel treatment with corn earworm and fall armyworm 
NPVs for protection of sweet corn. Hamm and Young (1974) demonstrated that corn earworm moths 
fed NPV could transmit the virus to their progeny by surface contamination of the eggs. 


Hamm (1982a) determined that the Helicoverpa armigera MNPV from the U.S.S.R. infected corn 
earworm, tobacco budworm, beet armyworm, and fall armyworm, but was about 200 times less 
virulent for fall armyworm than for corn earworm. Hamm (1982b) also discovered that the granulosis 
virus of H. armigera from South Africa was not restricted to the Heliothis/Helicoverpa complex, but 
would infect fall armyworm, beet armyworm, and cabbage looper in addition to corn earworm. 
However, this virus was not recommended for microbial control because of its slow kill and ability to 
interfere with faster acting NPVs. 


Early tests on application of entomopathogens in irrigation water were conducted by Hamm and Hare 
(1982) using a set sprinkler system. A fungus, Nomuraea rileyi, two species of microsporida, 
Vairimorpha heterosporum and Vairimorpha sp., and the fall armyworm NPV were applied to whorl 
stage corn for control of the fall armyworm. Elcar®, a commercial preparation of "Heliothis SNPV", 
was applied to silking corn for control of the corn earworm. All pathogens tested were infective when 
applied through the irrigation system. The fall armyworm NPV produced higher rates of larval 
mortality of fall armyworm and reduced the number of parasitoids emerging from collected larvae 
more than the Vairimorpha sp. and V. hetersporum, which generally did not kill fall armyworms until 
they were full grown larvae or pupae. In late-season tests, when there were continuous natural 
infestations of fall armyworm, two applications of NPV were sufficient to initiate epizootics. The 
viral epizootic extended to fall armyworm larvae collected from corn silks, even though no 


288 


eee rs 





applications had been made directly to the silks. Corn earworm larvae collected from Elcar-treated 
plots had significantly higher rates of mortality due to NPV than larvae from control plots and there 
was a significant reduction in damage to corn ears in the Elcar-treated plots. Hamm and Young 
(1985) applied fall armyworm NPV and Elcar to corn through a cable-tow irrigation system and 
through a center pivot irrigation system for control of fall armyworm and corn earworm. In the cable- 
tow experiment on seedling corn, the percent mortality due to NPV in fall armyworm collected after 
the first and second applications was quite low, but it increased considerably after the third 
application. There was very little difference in effectiveness of the oil and water formulations of the 
virus. Also, there was little difference in percent mortality of corn earworm larvae treated with Elcar 
or an oil formulation of the "Heliothis SNPV". The mean damage index was significantly higher in 
the control than in the treated plots with no significant difference between the Elcar treatment and the 
oil formulation of NPV. The center-pivot test with Elcar on silking stage corn showed rather low 
mortality (25.3%) due to NPV nine days after initial application but a substantial increase in larval 
mortality (36.7 to 63.3%) on days 11 and 16 as the virus spread through the corn earworm 
population. 


Hamm et al. (1986b) demonstrated that corn hybrids can affect the effectiveness of NPV for control 
of corn earworm. Elcar produced a greater reduction in number of corn earworm larvae on a corn 
hybrid with a tight husk extension than on a hybrid with a loose husk. 


Three different ascoviruses were found infecting field collected fall armyworm, corn earworm, and 
tobacco budworm larvae (Hamm et al. 1986a). These viruses were easily transmitted by injection or 
by parasitoids stinging infected and then noninfected larvae, but were only mildly infective per os. 
The virus interfered with development of parasitoid larvae in infected hosts without any sign of 
infecting the parasitoid (Hamm et al. 1985). Because ascovirus-infected larvae remain small for a 
long time, they are attractive to parasitoids for a prolonged period and can result in the loss of 
numerous parasitoid eggs. Therefore, ascoviruses should not be recommended for microbial control 
of noctuid pests. 


Hamm et al. (1988) reported the first baculovirus pathogenic to a parasitoid, Microplitis croceipes. 
This virus is associated with reduced rates of parasitism, failure of wasps to emerge from cocoons, 
and early mortality of adults that do emerge. This demonstrates the importance of checking parasitoid 
colonies for pathogens when importing them and when producing them for release or for research. 


NATIONAL CENTER FOR AGRICULTURAL UTILIZATION RESEARCH, PEORIA, IL. By 
Michael R. McGuire 


In 1940, the U.S. Congress provided for the establishment of four Centers located around the country 
to initiate research related to utilization of farm products. Since its inception, the National Center for 
Agricultural Utilization Research (NCAUR, formerly the Northern Regional Research Laboratory), 
located in Peoria, IL, has had a rich history in studying fermentation of various fungi and bacteria, 
including insect-pathogenic bacteria. Most of the early work with insect pathogens dealt with 
Bacillus popilliae, the causal agent of milky disease in the Japanese beetle. Some research was also 
done on biochemical aspects of Bacillus thuringiensis production but, more recently, work with 
encapsulation of B. thuringiensis in cornstarch has been the primary focus of the insect pathology 
work at the Center. 


Milky disease. Following Dutky's pioneering work on the description of B. popilliae (see section 
below on Insect Pathology Laboratory, Beltsville, MD), there was much interest in developing means 
to mass produce the bacterial spores under liquid fermentation conditions. Commercial methods used 
to produce B. popilliae involved the inoculation of spores into live grubs and then holding the grubs 
until death. The larvae were then dried and milled and the bacteria quantified and formulated. 


289 


Clearly, these methods were laborious, time consuming, costly, and not capable of producing enough 
spores to provide for wide-scale biological control of the beetle (Rhodes 1965). In 1961, scientists at 
the laboratory developed a research project whose goal was to develop a fermentation system for the 
production of B. popilliae spores. Though spores had been produced on solid media before, 
production was very low and unacceptable. Similarly, early work revealed that B. popilliae 
vegetative cells could be grown in high numbers easily in fermentation but spore production was not 
possible. Initial work was aimed at the physiology of the insect. Did biochemical changes take place 
during the infection process and were these changes related to sporulation? Furthermore could this 
knowledge be used in creating an artificial medium suitable for growth and sporulation (e.g., 
Shotwell et al. 1963)? An exhaustive series of studies on chemical changes occurring in the 
hemolymph of infected grubs revealed an overall reduction of lipids, proteins, and carbohydrates, a 
phenomenon observed for other insect-pathogen relationships. However, large populations of 
vegetative cells that sporulated were never observed in larvae, suggesting that non-nutritional factors 
were operating to regulate the sporulation process (Bennett and Shotwell 1973). In 1965, Rhodes 

et al. reported enhanced sporulation of B. popilliae on solid media. Although only 0.1-0.3% of the 
viable cells sporulated, this represented a considerable improvement over existing methods. Then in 
1966, Haynes and Rhodes reported the first production of B. popilliae spores in liquid medium. 
Although only approximately 2 million spores/ml (vs. 10 billion spores/ml hemolymph in vivo) were 
obtained, interest was high and the future looked promising. While conditions suitable for production 
of very large amounts of asporogenic cells were improved, the right combination of media 
ingredients necessary for increased spore production was never developed. The research conducted 
over the 15 years of the project resulted in the publication of more than 70 papers. Much basic 
information was obtained concerning infection processes, growth and sporulation in vivo, and 
physiological changes experienced by infected insects. Ultimately, however, the problem was not 
solved, and, despite numerous attempts by other research programs, B. popilliae in vitro spore 
production remains an enigma to insect pathologists and microbiologists. 


Bacillus thuringiensis. As a spin-off of the work with B. popilliae, research was also initiated on 
various aspects of B. thuringiensis (Bt) production and host range. Biochemical aspects of Bt 
fermentation, sporulation, and outgrowth (e.g., Nickerson et al. 1975) were studied and some 
interesting work was done on the susceptibility of Japanese beetle to Bt. Sharpe (1976) reported the 
first instance of a beetle susceptible to Bt, but follow-up research suggested that larvae may be 
susceptible only during certain periods of their life cycle and that susceptibility was closely 
correlated to mid-gut pH and presence of food in the alimentary tract (Sharpe and Detroy 1979). 





Formulation of bacteria in cornstarch. More recently, research aimed at extending the residual 
activity of entomopathogens (most notably B. thuringiensis) after application has resulted in the use 
of cornstarch as an encapsulating medium. Previous research indicated that B. thuringiensis remained 
viable for only a few hours if exposed to direct sunlight. Dunkle and Shasha (1988) developed a 
granular formulation that upon addition of suitable additives such as sunscreens or UV protectants 
(Dunkle and Shasha 1989) or feeding stimulants (Bartelt et al. 1990) could extend and enhance the 
activity of B. thuringiensis under field conditions (McGuire et al. 1990). Although granular 
formulations are suitable for some applications, sprayable formulations probably are used more 
frequently. McGuire and Shasha (1990) reported the development of a tank-mix formulation that 
upon spraying onto foliage would form a film that entrapped active ingredients (namely B. 
thuringiensis and associated sunscreens or feeding stimulants). As before, the formulation is 
composed of starch, but sugar is also added to enhance dispersing in the tank and subsequent 
adherence of the film to the leaf surface. Research is continuing on the formulation of insect 
pathogens at NCAUR and has been expanded to include viruses and fungi. 


290 


CORN INSECTS RESEARCH UNIT, ANKENY, IA. By Leslie C. Lewis 


Nosema pyrausta, originally described as Perezia pyraustae from the European corn borer (ECB) in 
France, was first collected in the U.S. (lowa and Ohio) by USDA-ARS entomologists W.G. Bradley 
and K.D. Arbuthnot (Steinhaus 1952). Researchers in ARS defined the role of this microsporidan as 
an important population regulator of ECB. It reduces the fecundity of adults (Zimmack and Brindley 
1957; Lewis et al. 1971; Sajap and Lewis 1988a) and kills larvae when applied to infested corn 
plants (Lewis and Lynch 1978; Lublinkhof et al. 1979; Lewis 1982). Also, Nosema pyrausta is 
compatible with many other pest insect population suppressants: parasitoids — Macrocentrus 
grandii (Cossentine and Lewis 1987), Lydella thompsoni (Cossentine and Lewis 1988), 
Trichogramma nubilale (Sajap and Lewis 1988b); predators — common green lacewing (Sajap and 
Lewis 1989); and host plant resistance (Lewis and Lynch 1976; Lynch and Lewis 1976). In these 
relationships, NV. pyrausta occasionally slightly reduces emergence, longevity, and fecundity of the 
beneficial insects but they easily coexist in the same ecosystem. 


Some of the early work to utilize Beauveria bassiana to control ECB was conducted by George York 
at the former European Corn Borer Laboratory. He produced B. bassiana on wheat bran and ground 
the substrate containing the B. bassiana making a crude formulation that was applied to corn. He 
obtained upwards of 90% reduction of ECB larvae in small experimental plots (York 1958). Little 
additional work was conducted with B. bassiana and ECB until the late 1980s. Work at the Corn 
Insects Research Unit defined an endophytic relationship between the corn plant and B. bassiana. 
Beauveria bassiana colonizes the plant, moves within the plant, and provides control of ECB (Bing 
1990; Lewis and Bing 1991; Bing and Lewis 1991). The mechanism of entry into the plant and 
movement within the plant is not known. 


Research on Bacillus thuringiensis (Bt) has been emphasized at the European Corn Borer 
Laboratory/Corn Insects Laboratory/Research Unit since the early 1960s. Many ARS entomologists 
researched ways of formulating Bt to increase efficacy. Raun (1963) and Raun and Jackson (1966) 
successfully controlled ECB larvae with granular formulations of Bt. Later, Lynch et al. (1977a and 
b, 1980) reduced performance variability of Bt by standardizing commercial products on an 
international unit basis, by varying the amount of Bt per unit volume of carrier and by using foam 
and more uniform formulations. This work was the impetus for commercialization of Bt for ECB 
management. Presently B. thuringiensis formulated products are used widely by hybrid seed 
producers and some commercial growers. 


Research was ongoing on basic aspects of B. thuringiensis and ECB while the developmental and 
application research was being pursued. Sutter and Raun (1966, 1967) described the histopathology 
of B. thuringiensis in ECB. They were the first to show that crystals damage the midgut epithelial 
cells allowing the gut contents to enter the hemocoel and cause a septicemia and death. Mohd-Salleh 
and Lewis (1982) demonstrated that neonate ECB larvae could be killed by crystals alone; however, 
older larvae had to be exposed to spores and crystals to maximize mortality. Lewis was a member of 
the international research group assembled by Howard Dulmage to investigate the spectrum of 
activity of B. thuringiensis (Dulmage 1981). This complete work is in its final stages of preparation 
and will eventually be published with Dulmage, Burges, and Lewis as editors. 


The ECB is one of the very few economically important insect pests from which no virus has been 
isolated. Nuclear polyhedrosis viruses from alfalfa looper (Lewis et al. 1977) and Rachiplusia ou 
(Lewis and Johnson 1982) are, however, virulent against this insect. Field efficacy has been 
demonstrated but, with the commercialization of B. thuringiensis, there has been little effort to 
develop a virus formulation for ECB management. 


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U.S. GRAIN MARKETING RESEARCH LABORATORY, MANHATTAN, KS. By William H. 
McGaughey 


Insect pathology research was initiated at the U.S. Grain Marketing Research Laboratory (USGMRL) 
in Manhattan, KS, in 1972 by W.H. McGaughey. This work was expanded in 1973 when L.A. Bulla, 
Jr., transferred to Manhattan. D.E. Johnson transferred to Manhattan in 1981, following the 
resignation of Bulla. 


McGaughey's studies initially focused on evaluation of the feasibility of controlling moth infestations 
in stored grain using either the Indianmeal moth granulosis virus or Bacillus thuringiensis (Bt) 
(McGaughey 1975b, 1976, 1978b, 1980, 1982; Nwanze et al. 1975). Both agents were found to be 
compatible with other stored grain treatments and were stable enough in the stored grain environment 
to provide long-term moth control (McGaughey 1975a, 1983; Kinsinger and McGaughey 1976). A 
surface-layer treatment method was developed that concentrated the dosage at the surface layer of the 
grain where the moth infestations occur (McGaughey 1978b, 1980; McGaughey and Dicke 1980). 
This approach greatly reduced the amount of material required for treating bulk grain and made the 
approach much more attractive economically. From the mid-1970s onward, McGaughey's research 
concentrated on Bt, which was a much more promising candidate for EPA registration. Extensive 
data were obtained on host spectrum and susceptibility, histopathological effects, environmental 
stability, compatibility with other treatments, fate of residues in milled grain products, and efficacy 
in different commodities (McGaughey et al. 1975, 1980; Kinsinger and McGaughey 1976, 1979a and 
b; McGaughey 1978a and c, 1982; McGaughey and Kinsinger 1978; Johnson and McGaughey 1984). 
Studies were also done on the susceptibility of stored-grain moths to various strains of Bt (Kinsinger 
and McGaughey 1978; Kinsinger et al. 1980). This work culminated in the registration of Bt for 
moth control in stored grain in 1979. This was the first registration of a microbial product for use on 
stored grain. (See McGaughey 1986b for a review of research on use of B. thuringiensis as a grain 
protectant.) 


Subsequently, McGaughey undertook large-scale field studies to evaluate various formulations and 
methods for applying Bt to bulk stored grain and to acquire data on the performance of the treatment 
under field conditions (McGaughey 1985b, 1986a). It was during the course of these studies that 
McGaughey discovered the potential for insect resistance to Bt 6-endotoxins (McGaughey 1985a; 
McGaughey and Beeman 1988). Subsequent studies involved efforts to characterize and elucidate the 
biochemical mechanisms of insect resistance to Bt and provided the first documentation of the role of 
midgut receptor binding in the mechanism of resistance (McGaughey and Johnson 1987; Han et al. 
1988; Johnson et al. 1990, 1991; Van Rie et al. 1990; Aronson et al. 1991). (See McGaughey 1990 
for a review of research on resistance.) 


The research on insect resistance has had far reaching effects on the course of research on Bt. It has 
provided a fruitful avenue for significantly expanding the understanding of the modes of action and 
specificity of Bt toxins. It has also raised questions regarding the long-term usefulness of Bt genes in 
producing insect-resistant transgenic plants. As a result, there has been a large increase in research on 
insect resistance to Bt in government, academia, and industry. This effort has led to the discovery of 
laboratory and field resistance in several important pest insects, including Colorado potato beetle, 
tobacco budworm, and diamondback moth, and has focused the attention of regulatory agencies and 
industry on the need to develop strategies for preventing resistance in order to preserve the 
usefulness of this valuable biological insecticide. 


Bulla's research on Bt strains when he was with ARS at the Northern Regional Research Laboratory 
(NRRL), Peoria, and at the USGMRL during the 1970s and early 1980s addressed a broad range of 
topics including nutritional requirements, metabolism, cytology of growth, sporulation and 
germination, and the biochemistry, molecular biology, and function of parasporal inclusion bodies 


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(Bulla et al. 1980). One of the first chemically defined synthetic media that allowed growth, 
sporulation, and parasporal crystal formation was developed by Nickerson and Bulla (1974). Various 
aspects of the intermediary metabolism of amino acids, polypeptides, carbohydrates, and lipids were 
described by Bulla's group (Bulla et al. 1970a and b, 1971a and b; St. Julian and Bulla 1971; Bulla 
and St. Julian 1972a and b; Nickerson et al. 1974). An ultrastructural analysis determined that the life 
cycle of Bt is characterized by three distinct major processes: vegetative cell division, spore 
development, and crystal formation (St. Julian et al. 1971; Afrikian et al. 1973; Bechtel and Bulla 
1976, 1982). More recent studies have focused on the isolation, activation and physical, chemical, 
and insecticidal properties of the parasporal inclusion body or 6-endotoxin (Sharpe et al. 1975; Bulla 
et al. 1976, 1977, 1979, 1981; Schesser et al. 1977; Schesser and Bulla 1978, 1979; Tyrell et al. 
1979, 1981a and b; Andrews et al. 1980). The mobilities of fatty acids in the plasma membrane 
during growth and sporulation were assessed in vivo using nuclear magnetic resonance (Bechtel et al. 
1985). The subcellular origin and physiological function of the parasporal crystal and spore coat 
proteins, as well as the gene for the lepidopteran protoxin were also studied (Stahly et al. 1978; 
Aronson et al. 1982; Held et al. 1982). Rocket immunoelectrophoretic and enzyme-linked 
immunoadsorbant assays were developed for detecting and quantifying parasporal inclusion body 
proteins from subspecies kurstaki and/or israelensis (Andrews et al. 1980; Wie et al. 1982). 


Johnson conducted research on Bt at the NRRL at Peoria beginning in 1972 and at the USGMRL 
after 1981. This research included many biochemical studies involving the bacterium and its crystal 
proteins, more recent studies concerning insect resistance to Bt, and a series of studies on the use of 
insect cell culture as a model system for investigating Bt insect toxicity. Certain insect cell lines 
respond to crystal protein from Bt, resulting in cell lysis. The response is specific and parallels insect 
larval mortality patterns from various subspecies of Bt. Several studies established the developmental 
patterns of insect culture response to Bt crystal protein (Johnson et al. 1980; Johnson 1981, 1987a; 
Johnson and Davidson 1984), and included development of a variant cell line that was resistant to 
crystal protein from Bt subspecies kurstaki (Johnson 1984). The system was used to measure the 
toxicity of wheat purothionins by Johnson and collaborators in 1984 (Jones et al. 1985). Several 
review articles summarized the work to date (Johnson 1987b, 1989). Some research still continues 
with insect cells involving their responses to specific cloned Bt toxin gene proteins. 


GULF COAST MOSQUITO RESEARCH LABORATORY, LAKE CHARLES, LA. By Tokou 
Fukuda 


In 1964, the ARS Entomology Research Division established a mosquito research laboratory in Lake 
Charles, LA, as a satellite laboratory to the Insects Affecting Man and Animals Research Laboratory 
of Gainesville, FL (now the Medical and Veterinary Entomology Research Laboratory). The purpose 
of the Lake Charles laboratory was to study the biology and ecology of the mosquitoes of the Gulf 
Coast area, especially Louisiana, in an effort to provide more effective means of mosquito control. 
Lake Charles was chosen because the Police Jury (County Commissioners) of Calcasieu Parish, LA, 
agreed to provide facilities with no charge. The original laboratory was located on the McNeese State 
College campus in a building shared with the mosquito research unit of the Louisiana Mosquito 
Control Association. D.B. Woodard was the first to arrive in the spring of 1964. H.C. Chapman 
arrived in October to recruit locally R.V. Cloud, F.E. Glenn, Jr., M.J. Gore, J.C. Hicks, and O.R. 
Willis to complete the original staff. A landmark year for the Lake Charles laboratory was 1967, 
when the laboratory became independent and assumed the name, Gulf Coast Mosquito Research 
Laboratory (GCMRL) with Chapman as the Investigations Leader. In 1970, the laboratory moved 
from McNeese State College campus to Chennault Air Force Base, where it remained until it was 
closed. 


The earliest research of Chapman and Woodard dealt with the biology of Louisiana mosquitoes, 
specifically the blood feeding and oviposition habits of local mosquitoes (Chapman and Woodard 


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1965). During this time the availability of large numbers of mosquitoes provided Chapman with the 
opportunity to begin parasite and pathogen investigations. He was introduced to this subject when 
assigned from 1961 to 1964 to the University of California Mosquito Research Laboratory in Fresno, 
California, where much of the pioneering work on mosquito parasites and pathogens was carried out 
by W.R. Kellen and T.B. Clark, and J.E. Lindegren. Beginning in 1965, a large number of papers 
were published on fungal infections by Coelomomyces in Louisiana mosquitoes (Chapman and 
Woodard 1966), additional hosts of mosquito iridescent viruses (Chapman et al. 1966), a 
microsporidan in a Louisiana mosquito (Chapman and Kellen 1967), and nematode parasites in 
Louisiana Culicidae and Chaoboridae (Chapman et al. 1967); other papers on parasites and 
pathogens were published by Chapman and the staff of the GCMRL. Along with the ability to detect 
pathogens, Chapman possessed the unique ability to colonize mosquitoes; through his efforts 
colonies of 17 species were maintained at the GCMRL (Chapman and Barr 1969; Chapman 1970). In 
addition to conducting his administrative duties as Location and Research Leader, Chapman authored 
over 40 publications during this period. After his retirement in 1981, Chapman was appointed as a 
non-paid USDA-ARS Consultant/Collaborator to the GCMRL. 


The first of several international projects that would involve GCMRL began in 1967. Chapman was 
asked by the United Nation's World Health Organization (WHO) to survey mosquito problems on 
Nauru Island in the South Pacific. During his survey he found several parasites and pathogens 
(Chapman 1967a), and reported on the mosquitoes found on the island and recommendations for 
their control (Chapman 1967b). 


Woodard conducted research on various aspects of mosquito biology, parasites and pathogens. Some 
of Woodard's research on biology of mosquitoes include blood volumes ingested (Woodard and 
Chapman 1965) and egg hatchability of floodwater mosquitoes (Woodard et al. 1968; Woodard and 
Chapman 1970). His research began in 1968 with laboratory studies of the mosquito iridescent virus 
(Woodard and Chapman 1968) and extended to nematode studies where he demonstrated 
development of resistance of mosquitoes to nematodes (Woodard and Fukuda 1977). He also 
established a mermithid nematode in a field population of anopheline mosquitoes (Woodard 1978). 
Woodard left the GCMRL in 1976 to take a position as an entomologist with the ARS Screwworm 
Research Laboratory in Tuxtla Gutierrez, Mexico. 


J.J. Petersen joined the staff of the GCMRL in 1966 after completing his Ph.D. at the University of 
Utah. Although he was recruited to study mosquito biology, his most important contribution was to 
the development of mermithid nematodes for mosquito control. Assisted by O.R. Willis, he compiled 
a list of potential hosts for mermithids (Petersen et al. 1969). He also developed mass rearing 
methods for the mermithid nematode Romanomermis culicivorax (as Reesimermis nielseni) (Petersen 
and Willis 1972a). The ability to mass rear the nematode made possible preliminary field tests in 
California and Louisiana (Petersen and Willis 1972b; Petersen et al. 1972). WHO also sponsored a 
field release of the nematode against the southern house mosquito (as Culex pipiens fatigans) in 
Bangkok, Thailand (Chapman et al. 1972). A large field test of a 40-hectare lake in El Salvador 
involving numerous applications of the nematode over seven weeks resulted in near eradication of 
the anopheline malarial vector (Petersen et al. 1978a and b; Willis et al. 1980). Petersen completed 
an extensive study of oviposition responses of Louisiana mosquitoes (Petersen 1969; Petersen and 
Chapman 1970; Petersen and Willis 1970, 1971). He continued to work with mermithid nematodes 
and had over 50 publications by 1978, when he transferred to the Livestock Insects Research 
Laboratory in Lincoln, NE. 


T.B. Clark and Tokuo Fukuda were added to the staff of the GCMRL in 1967 and continued the 
parasite and pathogen work that Clark had started in California at the University of California 
Mosquito Research Laboratory at Fresno. During his short time at the GCMRL, Clark's contributions 
were his entomopathogenic virus research with Louisiana mosquitoes (Clark and Chapman 1969; 


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Clark and Fukuda 1971a) and the description of a new microsporidan in a Louisiana mosquito (Clark 
and Fukuda 1971b). Clark returned to California in 1970 to accept a faculty position at Fresno State 
University. He rejoined the USDA when the Western Insects Affecting Man and Animals Research 
Laboratory was relocated to Fresno. Clark's untimely death occurred in 1984 while on a field trip to 
Mexico for the Insect Pathology Laboratory of the Plant Protection Institute in Beltsville, MD (see 
section below). 


After the departure of Clark, Fukuda continued viral transmission and pathogenicity studies on 
mosquitoes (Fukuda 1971; Fukuda and Chapman 1973; Fukuda and Clark 1975). He and Woodard 
collaborated on hybridization studies of saltmarsh and floodwater mosquitoes (Fukuda and Woodard 
1974a and b). Fukuda's research on parasites and pathogens included a report of a new protozoan 
parasite in mosquitoes (Fukuda et al. 1976). 


R.E. McLaughlin transferred to the GCMRL from the Boll Weevil Research Laboratory in Starkville, 
MS. McLaughlin began his work testing the effectiveness of Bacillus thuringiensis serotype H-14 
(subspecies israelensis) (Bti) against the southern house mosquito (McLaughlin and Fukuda 1982), 
then turned his attention to rice field mosquitoes (McLaughlin et al. 1982; McLaughlin and 
Billodeaux 1983; McLaughlin and Vidrine 1984a). McLaughlin also developed a new method for 
dispensing liquid formulations of Bti into rice fields (McLaughlin 1983; McLaughlin and Vidrine 
1984b), and contributed to the development of a standard bioassay to determine Bti potency 
(McLaughlin et al. 1984). 


J.J. Becnel began his career with the USDA at the GCMRL in October 1980 after obtaining a M.S. 
degree at McNeese State University. Becnel's thesis research on the relative potency of combinations 
of chemical larvicides with Bti was done at the GCMRL. In 1982, Becnel was given the task of 
overseeing the operation of the newly installed electron microscope. After transfer of personnel of 
GCMRL to the Insect Affecting Man and Animals Research Laboratory in Gainesville, FL, he 
obtained a Ph.D. in entomology from the University of Florida in 1989. 


E.I. Hazard transferred to the GCMRL in 1981 after 18 years of distinguished research at the Insects 
Affecting Man and Animals Research Laboratory in Gainesville, FL. Hazard continued his 
microsporidan work with the assistance of Fukuda and Becnel and completed a life cycle study of 
Culicosporella lunata in Culex restuans (Hazard et al. 1984) and also described gametogenesis and 
plasmogamy in microsporida (Hazard et al. 1985). He was instrumental in investigations leading to 
the discovery that a copepod intermediate host was required to complete the life cycle of 
Amblyospora, a microsporidan parasite of mosquitoes (Sweeney et al. 1985). Hazard became 
Location Leader of the GCMRL after Chapman's retirement in 1981. He initiated an effort to relocate 
the GCMRL to Louisiana State University in Baton Rouge, LA. Negotiations with LSU officials and 
the ARS Mid-South Area Office for the use of facilities were underway when Hazard's sudden death 
in March 1985 brought an end to the relocation plan. 


Fukuda was named Acting Location Leader until a permanent Location Leader was installed. 
However, a decision was soon made to consolidate the GCMRL efforts with that of the pathology 
unit of the Gainesville laboratory and transfer the GCMRL personnel to Gainesville. The GCMRL 
was closed in October 1985 with the transfer of McLaughlin, Willis, Becnel, and Fukuda to 
Gainesville, FL (see above). 


Because of the research and progress in the area of biological control of mosquitoes, in 1972 the 
GCMRL was named a WHO Collaborating Laboratory for Pathogens and Parasites of Mosquitoes 
(one of three in the world). In 1977, both Chapman and Petersen were appointed by WHO to the 
Scientific Working Group on Biological Control of Vectors (SWG/BCV) which periodically met in 
Geneva, Switzerland. These appointments involved numerous short-term consultantships to 


295 


developing countries. Because of the stature of GCMRL, Chapman was appointed for seven years 
(three as chairman) to the Steering Committee of the WHO/SWG/BCV. 


The GCMRL, although relatively small, produced nearly 200 publications on mosquito biology and 
biological control in its 21-year existence and became known worldwide for its pioneering work in 
mosquito biological control. The success of the GCMRL was in no small part due to the field 
personnel, Cloud, Glenn, and Willis, who daily provided the material for examination or 
experimentation. The personnel proved not only to be outstanding scientists but contributed their 
services to mosquito control organizations. Chapman served as a member of the board of directors, 
vice-president and president of both the American Mosquito Control Association and the Louisiana 
Mosquito Control Association; Fukuda served as a member of the board of directors, vice-president 
and president of the Louisiana Mosquito Control Association; and Woodard served on the board of 
directors of the Louisiana Mosquito Control Association. 


NORTHEAST PLANT, SOIL AND WATER LABORATORY, ORONO, ME. By Richard A. 
Humber 


See Ithaca, New York. 
BEE RESEARCH LABORATORY, BELTSVILLE, MD. By Hachiro Shimanuki and David A. Knox 


Insect pathology in the USDA officially began in 1907 when the Bureau of Entomology employed 
G.F. White as a bee pathologist. The first Division of Bee Culture Laboratory was located in 
Somerset, MD, now a section of Chevy Chase, which borders on Washington, DC. The Laboratory 
was re-located a number of times in the Washington area until 1939 when it was moved to Beltsville, 
MD, where it is currently located. Although the laboratory was primarily known for its bee disease 
work, a number of its scientists who made their reputations in other specialties also made 
contributions to bee pathology. These include such names as E.F. Phillips, J.1. Hambleton, and W.J. 
Nolan. 


G.F White was a pioneer, not only in bee pathology but also in insect pathology. He was the first in a 
long line of bee pathologists beginning a tradition of excellence in bee pathology which continues 
today at the Bee Research Laboratory in Beltsville. White differentiated American and European 
foulbrood diseases (White 1906); however, it was E.F. Phillips, in the introduction to White's (1906) 
publication on bacteria in the apiary, who named the diseases. White published monographs on 
American foulbrood (1907, 1920a), European foulbrood (1920b), Nosema disease (1919), and 
sacbrood (1917). After two years in the military, White returned to the Bureau of Entomology as a 
specialist on insect diseases. Later he was transferred to Moorestown, NJ, where he began a study on 
the diseases of the Japanese beetle in 1933. In less than two years, he was a member of a team that 
identified the "milky disease" as a means to control this important pest insect. White worked in 
Moorestown until his death in 1937. 


A.P. Sturtevant was employed by the Bureau of Entomology, Bee Research Division, Somerset, MD, 
in 1916 to conduct studies on the etiology of bee diseases and the pathology of Nosema disease of 
honey bees. He was transferred to the Intermountain Bee Culture Field Laboratory, Laramie, WY, in 
1926. Sturtevant was known primarily for his research on bee diseases, in particular the etiology of 
American foulbrood (Sturtevant 1924), a method to determine the presence of Bacillus larvae spores 


in honey (Sturtevant 1932, 1936), and many other papers on the diagnosis of bee diseases (Burnside 
et al. 1949). 


C.E. Burnside began his career with honey bees in 1924 with the USDA Bureau of Entomology. He 
spent the summers of 1924—26 at the University of Michigan studying relative virulence of various 


296 


species of fungi and bacteria in relation to brood and adult bee diseases. Burnside was transferred in 
1939 to the Divisional Headquarters of the Bureau of Entomology and Plant Quarantine, Bee Culture 
Unit in Beltsville, where he was responsible for the diagnosis of brood and adult bee diseases for the 
USDA. In 1942, due to World War II and the need to realign personnel, he was transferred to 
Laramie, WY. Burnside was noted for his research on fungi associated with honey bees (Burnside 
1930), control of American foulbrood (Burnside 1931), bacteria associated with European foulbrood 
(Burnside 1934), and on septicemia (Burnside 1928), purple brood (Burnside 1935), chronic bee 
paralysis (Burnside 1945), and Nosema disease (Burnside and Revell 1948). Burnside died in 1949. 


E.C. Holst was employed by the Beekeeping and Insect Pathology section of the Bureau of 
Entomology and Plant Quarantine of USDA in 1938. He was stationed in Laramie, WY, until 1942 
when he was transferred to the Bee Culture Laboratory at the U.S. Agricultural Research Center in 
Beltsville. Holst was noted for the development of the “milk test” used by some to make a 
differential diagnosis of American and European foulbrood diseases (Holst 1946). In addition, Holst 
discovered the antibiotic, larvacin, produced by Bacillus larvae, the etiologic agent of American 
foulbrood disease (Holst 1948). Holst retired in 1951 and died in 1954. 


A.S. Michael started his career at Beltsville in 1948 in the Bee Culture Laboratory. He became 
Laboratory Leader in 1958 and was Investigations Leader for bee diseases from 1962 to 1965. From 
1965 to 1972, he served as the Assistant Branch Chief of the Apiculture Research Branch of ARS' 
Entomology Research Division. When ARS was reorganized in 1972, he became the first Laboratory 
Chief of the Bioenvironmental Bee Laboratory at Beltsville. Michael was recognized worldwide as 
an expert on bee diseases and he began the early logistical measures in preparation for the expected, 
eventual establishment of parasitic mites in the U.S. (Michael 1961, 1963). He was the first to 
recognize the potential use of ethylene oxide for the control of bee diseases (Michael 1964). Michael 
retired in 1975. 


Hachiro Shimanuki started his career with the ARS Bee Disease Investigations Laboratory, Laramie, 
WY, in 1963. Three years later, he was transferred to the Bee Culture Laboratory in Beltsville. 
Shimanuki served in various capacities in Beltsville and is currently the Research Leader of the Bee 
Research Laboratory. Shimanuki's contributions have been divided between administration and 
research. He has served as the principal liaison between ARS and APHIS, Food and Drug 
Administration (FDA) and the EPA. His research is primarily on the etiology and control of bee 
diseases and bee nutrition. Recently he has been associated with the control of parasitic mites and the 
Africanized honey bee. Among his accomplishments are the use of high velocity electron beams to 
control bee diseases (Shimanuki et al. 1984), conduction of the first comprehensive survey for 
tracheal mites (Shimanuki et al. 1983) and coauthorship of a handbook on methods of diagnosing bee 
diseases (Shimanuki and Knox 1991). 


Thor Lehnert was associated with the Bee Culture Laboratory in Beltsville from 1959-81, except for 
the period 1968-70 when he was stationed in Baton Rouge, LA. He was in charge of bee disease 
diagnosis until April 1976 when D.A. Knox took over that service. In 1981, Lehnert transferred to 
the USDA National Agricultural Library. His research was primarily on the control of Nosema and 
European foulbrood diseases (Shimanuki et al. 1969; Lehnert and Shimanuki 1973). 


G.E. Cantwell spent most of his career with the ARS Insect Pathology Laboratory in Beltsville (see 
below) and was assigned to the Bioenvironmental Bee Laboratory from 1977 to 1980 only. Cantwell 
conducted research on the use of temperature extremes (Cantwell and Lehnert 1968), ethylene oxide 
(Cantwell et al. 1975), and carbon dioxide (Cantwell and Smith 1970) for the control of Nosema 
disease and the greater wax moth. 


297 


J.D. Vandenberg joined the Bioenvironmental Bee Laboratory in 1983 and was transferred to Logan, 
UT, in 1987. While in Beltsville, Vandenberg conducted research on laboratory rearing of honey 
bees (Vandenberg and Shimanuki 1987), the control of greater wax moth (Vandenberg and 
Shimanuki 1990a), safety of biorational pesticides for honey bees, and the half-moon syndrome of 
honey bees (Vandenberg and Shimanuki 1990b). 


D.A. Knox began his career in the Bee Culture Laboratory in 1961 while enrolled as an 
undergraduate student. His research included safety testing of candidate biological control agents 
(Knox 1970). He did some of the first research on combining ethylene oxide fumigation and feeding 
oxytetracycline hydrochloride to reduce the recurrence of foulbrood diseases in honey bee colonies 
(Knox et al. 1976). Currently, Knox is in charge of the bee disease diagnostic service and is a 
coauthor of a handbook on bee disease diagnostic techniques (Shimanuki and Knox 1991). 


T.B. Clark joined the Bioenvironmental Bee Laboratory in 1975 and transferred to the Insect 
Pathology Laboratory in 1981. He died in 1984 while on a collecting trip in Mexico. Clark made 
some significant contributions in bee pathology during the short time he worked on bees. He showed 
that the so-called rickettsial disease of honey bee was in reality a filamentous virus (Clark 1978). In 
addition, he identified a disease of honey bees caused by a spiroplasma which he later showed was 
found in the nectar of some plants frequented by the honey bees (Clark 1977). 


E.W. Herbert, Jr., began his career with the USDA in 1966, as a part-time technician, and, except for 
three years with the military, he worked on honey bee nutrition (Herbert 1991) and its effect on 
European foulbrood disease (Herbert and Shimanuki 1982). When parasitic mites were discovered in 
the U.S., Herbert developed treatments against Acarapis woodi (Herbert et al. 1987) and Varroa 
jacobsoni (Herbert et al. 1988a). Herbert died in 1988 at the age of 45. 


W.A. Bruce was transferred to the Beneficial Insects Laboratory (later Bee Research Laboratory) in 
1987. His primary assignment was to develop laboratory rearing methods for honey bee parasitic 
mites. In addition, Bruce has worked on the control of parasitic mites (Herbert et al. 1988b) and the 
role of parasitic mites in the transmission of bee pathogens (Bruce et al. 1991). 


N.W. Calderone joined the Bee Research Laboratory in 1992. His primary responsibility was to 
conduct research on the biology and control of parasitic mites. Calderone has concentrated on two 
approaches to mite control, a genetic solution and a chemical solution using botanical compounds 
that are environmentally safe. In addition to his work on mite control, Calderone is developing 
procedures to sample for mite diseases (Calderone and Shimanuki 1992) and will study the host- 
seeking behavior of parasitic mites. 


Mercedes Delfinado-Baker was associated with the bee laboratory from the late 1960s to the late 
1980s as a research associate, acarologist. She performed all the authoritative identification of mite 
samples received by the laboratory from all over the world. In fact, it was she who made the official 
identification of the honey bee mite, Acarapis woodi, in Mexico and later the identification of A. 
woodi (Delfinado-Baker 1984) and Varroa jacobsoni in the U.S., and was the first to report the 
occurrence of the mite Melittiphis alvearius in this country (Delfinado-Baker 1988). 


INSECT PATHOLOGY LABORATORY/INSECT BIOCONTROL LABORATORY, 
BELTSVILLE, MD. By Jean R. Adams 


The USDA became involved in research on microbial diseases for the control of insect pests many 
years ago with the research of S.R. Dutky at Moorestown, NJ. The Japanese beetle was discovered in 
Riverton, NJ, and soon became an economic pest in part because of the absence of natural enemies. 
In a search for diseased grubs, Dutky discovered a microorganism, later named Bacillus popilliae 


298 


Dutky, that successfully controlled the grubs of this pest (Dutky 1940, 1941a, b and c, 1963; White 
and Dutky 1940). He proceeded to develop procedures for mass production of the microorganism 
(Dutky 1942a) in grubs by injection with a microinjector which he developed (Dutky and Fest 1942), 
since it was not infectious per os, and he demonstrated that the organism produced was indeed B. 
popilliae (Dutky 1947). Then he developed a formulation of spore dust and worked out application 
procedures for its effective use (Dutky 1942b). Large areas of turf were treated, e.g., the mall 
grounds in Washington, DC, airport grounds, golf courses, and many communities elected to treat all 
areas containing turf. Bacillus popilliae has proved to be a very effective method to control the 
Japanese beetle and is still marketed today (see also Dutky 1992). Dutky and the Insect Pathology 
Unit at Moorestown was moved to Beltsville, MD, in 1954, with the formation of the Insect 
Pathology Pioneering Research Laboratory. 


A.M. Heimpel came to the Insect Pathology Pioneering Research Laboratory in 1961 as Principal 
Insect Pathologist and later as Laboratory Chief. He was deeply committed to the field of insect 
pathology and was an inspiration to all who knew him. As leader of the laboratory, he always had 
time to listen, to guide and to encourage each person through difficult times in their research. He was 
intensely interested in the mode of action of insect pathogens, perhaps as a result of earlier studies 
with Tom Angus and other colleagues at the Insect Pathology Research Institute at Sault Ste Marie, 
Ontario, Canada. As R.M. Faust pursued studies to unravel the events in the insect gut following 
ingestion of Bacillus thuringiensis (Bt), Heimpel also advised and encouraged Russell Travers, 
Toshihiko lizuka, and others on further studies on the genetic mechanisms controlling 6-endotoxin 
production. The knowledge obtained was crucial to genetic engineering studies that would come after 
his untimely death in 1979. He was also very interested in searching for new insect pathogens, mass 
rearing insects free of disease, and histological/cytological studies and cooperated with J.R. Adams 
in these areas of research. J.V. Thompson, previously with the Japanese beetle project, was 
reassigned to the disease diagnosis service under Heimpel's direction for several years before his 
retirement. He studied a new nuclear polyhedrosis virus of the almond moth (Thompson and 
Redlinger 1968) and a pathogenic strain of Bacillus cereus isolated from the cigarette beetle 
(Thompson and Fletcher 1972). Heimpel was awarded the USDA Superior Service Award in 1966 
and the National Aeronautics and Space Administration (NASA) Group Award in 1970 for 
participation in studies in which lunar material returned from the first manned landing was examined 
for the presence of replicating agents which might be harmful to life on earth. 


Heimpel was involved in safety testing of insect pathogens and developed testing protocols that were 
prerequisites for the registration of microbial agents. He also prepared two large documents for 
submission to the U.S. Environmental Protection Agency, one on the exemption from the 
requirement of a tolerance for use of AcMNPV on lettuce and cabbage in cooperation with P.V. Vail, 
another ARS insect pathologist. Another was also prepared for the exemption from the requirement 
of a tolerance for use of milky spore disease bacterium, B. popilliae, on pastures. For further details 
of Heimpel's innumerable contributions to the Insect Pathology Laboratory (IPL), to the Society of 
Invertebrate Pathology of which he was a founding member, Secretary-Treasurer, Trustee and later 
Vice President, and his participation in national and international meetings and symposia the reader 
is referred to Faust's account of Heimpel's accomplishments (Faust 1984). 


G.E. Cantwell came to the USDA in 1959 initially working with Dutky. After Heimpel became the 
leader of the laboratory, Cantwell's primary efforts were in developing strains of Bt for controlling 
the gypsy moth (Cantwell et al. 1961), greater wax moth (Cantwell and Shieh 1981), sciarid larvae 
(Cantwell and Cantelo 1982a), Colorado potato beetle (Cantwell and Cantelo 1984), and the Mexican 
bean beetle (Cantwell and Cantelo 1982b). He developed and produced a kit for the collection and 
shipment of pathogens for use by the World Health Organization (Cantwell and Laird 1966) and 
organized the "Registry of Tumors in Lower Animals" in conjunction with the National Institutes of 
Health and housed at the Smithsonian Institution of Washington, DC (Cantwell et al. 1968). He 


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developed several techniques for controlling diseases and pests of the honey bee, including Nosema 
apis (Cantwell and Lehnert 1968; Cantwell and Smith 1970; Cantwell et al. 1972; Lehnert and 
Cantwell 1978). Cantwell retired in 1985. 


R.M. Faust came to the IPL in 1961 as an agricultural research technician while completing his B.S., 
M.S., and Ph.D. degrees in entomology, microbiology, and biochemistry. Over the years, his research 
dealt with such subjects as the chemical basis of the cell-cementing substances of insect tissues 
(Faust et al. 1967; Faust and Dougherty 1969), in vitro chemical reaction of 6-endotoxin of Bt (Faust 
1968), the standardization of the 6-endotoxin produced by several varieties of Bt (Faust et al. 1971a 
and b), and the spectrographic elemental analysis of Bt and fall armyworm nuclear polyhedrosis virus 
(SfMNPV) (Faust et al. 1973). 


Faust then studied the mode of action of the 6-endotoxin of Bt (Faust et al. 1974a and b) and the 
effects of Bt variety kurstaki 6-endotoxin on isolated lepidopteran mitochondria (Travers et al. 

1976). The extrachromosomal DNA in several varieties of Bt was examined as well as the occurrence 
of resistance to neomycin and kanamycin in B. popilliae and certain serotypes of Bt (Faust et al. 
1979; Faust and Travers 1981). Extrachromosomal DNA was isolated and purified from serotypes of 
Bt pathogenic to Lepidoptera and Diptera larvae (Iizuka et al. 1981a) and comparative profiles of 
plasmid DNA were obtained from single and multiple crystalliferous strains of Bt subspecies 
kurstaki (lizuka et al. 1981b) and Bt subspecies darmstadiensis (lizuka et al. 1983). The comparative 
morphology and size distribution of the parasporal crystals from various strains of Bt were also 
reported (Faust et al. 1982). 


Between 1982 and 1984, Faust's research emphasis was aimed at the characterization and 
comparative analysis of plasmid DNA and parasporal crystal structure from a diverse array of 
entomopathogenic bacilli related to cooperative efforts on gene manipulation and transfer (Abe et al. 
1982, 1983, 1984; Wie et al. 1984). Faust also prepared chapters on the insecticidal protein genes of 
Bt (Faust and Adams 1989a), the plasmid biology of Bt (Faust et al. 1989), and the present and future 
strategies for improvement of Bt through gene manipulation (Faust and Adams 1989b). In 1988, he 
became a member of the ARS National Program Staff and is presently (1993) serving in that position 
covering basic insect biology and crop protection with special emphasis on pesticide resistance, 
insect neurohormones, and genetic sexing. 


P.A.W. Martin joined IPL in 1981. The most successful aspect of her research has been the discovery 
of new Bt strains. She developed a method to isolate Bt spores from the environment, specifically 
from soil (Martin et al. 1985; Travers and Martin 1990). The method, named acetate selection, has 
become a standard procedure for Bt isolation (Travers et al. 1987). Samples were collected from all 
over the world (Martin and Travers 1989), and, because of the large number of samples received, it 
became necessary to develop novel techniques to process and characterize the isolates (Travers et al. 
1987). From this research, Martin has received a patent on three Bt strains effective against 


Lepidoptera. She also demonstrated that Bt occurs everywhere and not necessarily in association 
with insects. 


J.R. Adams came to IPL in 1962. One of her first projects was to study ten samples of cabbage looper 
NPVs collected from five different geographical areas in the U.S. Morphological differences were 
noted between the virus samples. Some polyhedra contained single virions (SNPV) embedded in the 
polyhedron matrix while others contained bundles of virions (MNPV) embedded in the polyhedron 
matrix (Heimpel and Adams 1966). Adams also described several viruses for the first time including: 
NPV from the zebra caterpillar (Adams et al. 1968); NPV from almond moth (Adams and Wilcox 
1968); CPV from pink bollworm (Ignoffo and Adams 1966); an iridescent virus and an ascovirus 
from the bollworm/corn earworm (Adams et al. 1979a; Stadelbacher et al. 1978); rhabdovirus-like 
particles in the house cricket (Adams et al. 1980); and two virus-like particles in the Mexican bean 


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beetle (Adams et al. 1979b). Histopathological investigations were performed on each of the above 
host species noting the susceptible tissues, etc.; these were summarized in the Atlas of Invertebrate 
Viruses (Adams and Bonami 1991). 


Cytological investigations also revealed that baculoviruses have two forms of virions. The virions 
occluded in polyhedra (PDV = polyhedra derived virions) are produced in susceptible cell nuclei and 
are involved in the process of invasion as PDVs are released from the polyhedra or VOs (viral 
occlusions) due to the alkalinity of the midgut. In the lumen of the midgut, the PDVs attach to 
microvilli and are taken into the nuclei of the midgut columnar cells where an initial cycle of 
replication usually occurs in the most virulent NPVs. The newly produced virions then bud through 
the basal plasma membrane where a part of the envelope which is acquired is modified with 
glycoprotein spikes or peplomers. These virions, called ECVs (extracellular virus), are involved in 
the systemic infection as ECVs attach to plasma membranes of cells of susceptible tissues and are 
taken in by a process of viropexis. The unenveloped nucleocapsids gain entry to nuclei where a cycle 
of viral replication occurs producing PDVs which are occluded in VOs or polyhedra (Adams et al. 
1977; Adams and McClintock 1991). 


A technique was developed for determining the osmolality of the hemolymph of insects; osmolality 
was measured for ten insect pest species (Adams and Wilcox 1973). This information aided the 
development of fixatives for insect tissues which would give optimal preservation, as well as the 
modification of insect cell culture studies for optimal cell growth and/or polyhedra production for 
each insect species. A technique for detecting defective or cracked VOs was developed by comparing 
scanning electron microscope (SEM) with dark field STEM (scanning transmission electron 
microscope) images of the samples (Adams 1985). By observation of thin sections of VOs, a 
quantitative technique was developed in which differences in numbers of virions/VO and numbers of 
virions/virus bundle were correlated with differences noted in mortality data (Tompkins et al. 1988a, 
1991). Several SEM techniques were adapted and compared in order to obtain the maximum 
resolution of VO samples (Adams and Wilcox 1982). 


A rickettsia-like organism has been identified in colonized cat fleas from one source but not other 
sources checked. Histopathological examinations revealed the microorganisms in the midgut, 
tracheal matrix, muscle, hypodermis, ovaries, and epithelial sheath of the testes (Adams et al. 1990). 


S.J. Louloudes, a biochemist, transferred from the Insect Physiology Laboratory to the IPL in 1964. 
In early studies, he demonstrated that insect cells could not synthesize sterols and that fetal bovine 
serum added to the insect cell culture media was the source of sterols for the cells (Vaughn et al. 
1971). His research focused on sterols and fatty acids of insect tissues and insect cell cultures, 
working with J.L. Vaughn and R.H. Goodwin in the development of insect cell culture media until 
his untimely death in 1984 (Goodwin et al. 1970, 1973; Vaughn et al. 1971; Samish et al. 1985). 


In 1965, J.L. Vaughn joined the Insect Pathology Laboratory and began studies into the culture of 
insect cells and their use in the study of viruses with associates M.S.M. Stanley and R.H. Goodwin. 
At this time, the first cell lines from invertebrates had just been reported by Tom Grace (Grace 1962) 
in Australia. Early studies at Beltsville concentrated on developing an understanding of the tissues 
that would provide growing cells (Stanley and Vaughn 1968) and the development of suitable media 
and methods for establishing primary cultures (Goodwin 1975). Numerous cell lines were established 
from important insect pests in the U.S., e.g., corn earworm, gypsy moth (Goodwin et al. 1978), and 
fall armyworm (Vaughn et al. 1977). The cell line IPLB-SF-21AE has been the most important of 
these early cell lines as it was the parent line of several clones that have been used widely for the 
culture of genetically-engineered baculoviruses. The early cell lines from gypsy moth developed by 
Goodwin were the foundation of the important studies by E.M. Dougherty and D.E. Lynn that 
followed. Several new media formulations were developed during this time by Goodwin, one of 


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which, IPL-41, later modified by Weiss et al. (1981), is sold commercially. It was during this time 
that the use of cell cultures for the study of insect viruses became accepted. Among the contributions 
from this Laboratory, in addition to the cell lines, were methods for assaying insect viruses by end 
point dilution (Vaughn and Stanley 1970) and characterization of extracellular virus. 


E.M. Dougherty came to the IPL in 1966 as a student and later worked as a technician as he pursued 
advanced degrees at the University of Maryland. The research for his M.S. degree involved 
identification and characterization of the ECV phenotype (Dougherty et al. 1975). His Ph.D. research 
continued investigations on the ECV relationship to cell attachment parameters and the effects of 
various inhibitors on macromolecular synthesis on both ECV and PDV phenotypes (Dougherty et al. 
1981). Attempts to establish in vitro replication of granulosis viruses were unsuccessful; however, a 
unique cell line, TnR’, was initiated. The long eclipse stage of granulosis virus in vivo was described 
as was the effect of granulosis virus infectivity on hormonal titers in the insect (Dougherty et al. 
1989). 


Over the last decade Lymantria dispar NPV (LdMNPV) has been the focus of Dougherty's studies as 
he has collaborated with Martin Shapiro, D.E. Lynn, Tom McClintock (as a graduate student and 
then as a Post Doctoral Fellow), Post Doctoral Fellows David Guzo and Harold Rathburn, and 
support scientists Kim Guthrie and Martin Stranathan. The LdMNPYV virus-host interactions have 
been described and compared to the prototype Autographa californica MNPV (AcMNPV). LdMNPV 
replication has been described (McClintock et al. 1986a and b) and the genome mapped (McClintock 
and Dougherty 1988). Semi-permissive replication has been obtained with AcMNPV in IPLB-Ld- 
652Y cell cultures while several other gypsy moth cell lines were nonpermissive (McClintock et al. 
1986a). Both the IPLB-Ld-652Y cell line and the IPL-LdFB cell line, also semi-permissive for 
AcMNPYV replication, have been investigated at the transcriptional level (Guzo et al. 1992). Viral 
transcription appears normal by all criteria tested; however a translational block occurs in both 
systems. Guzo has recently discovered a macromolecular protein synthesis inhibition factor (MSIF) 
which effects cell translation and may be the AcMNPV 64-kDa glycoprotein or some component or 
complex of this protein (Guzo et al. 1991a and b, 1992). Rathburn investigated the making of a 
baculovirus expression vector from this system. The systems developed by Lynn, Shapiro, and 
Dougherty have been or are currently being licensed by American Cyanamid as the first in vitro 
commercial baculovirus production system. 


G.J. Tompkins came to IPL while a student and completed his B.S. and M.S. degrees, served in the 
U.S. Army in Vietnam, returned and then completed his Ph.D. His area of research included 
immunology, isolation, purification, and testing of new baculovirus isolates. He demonstrated 
conclusively that the MNPVs could replicate in more than one species, e.g., Trichoplusia ni MNPV 
replicated in corn earworm, but the Helicoverpa zea SNPV (HzSNPV) would not replicate in cabbage 
looper (Tompkins et al. 1969). He demonstrated and reported for the first time that 
microencapsulation of baculoviruses with sunscreens significantly improved the efficacy of viruses 
used for control of cabbage loopers and imported cabbageworms on collards (Tompkins et al. 
1988b). Tompkins also showed that the virulence of baculoviruses that have multiple host ranges can 
be altered when serially passaged in alternate susceptible hosts and permissive cell lines (Tompkins 
et al. 1988a) and reported for the first time that the virulence and internal morphology of MNPVs are 
_ altered when serially passaged in alternate susceptible hosts (Tompkins et al. 1981). He also reported 
for the first time that the addition of liposomal material to the cell culture medium used in culturing 
baculoviruses maintained the virulence of the MNPVs after being serially passaged in the cell lines. 
This demonstrated that some cell culture media may be deficient in required nutrients to maintain 
virulence in progeny virus harvested from the cell culture medium (Tompkins et al. 1991). 


R.H. Goodwin joined IPL in 1968. He initiated cooperative studies with Adams and Louloudes 
leading to repeatable baculovirus replications in a noctuid moth pupal tissue cell line isolated from 


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the fall armyworm by Vaughn (Goodwin et al. 1970, 1973). He extended his cell culture virus 
replication studies to include the investigation of cell lines from other noctuid species of economic 
importance in various tissue culture media he developed (Goodwin et al. 1976). He initiated 
investigations within ARS on gypsy moth in vitro production systems by developing a number of 
pupal tissue-derived cell lines which had differing responses to various (homologous and 
heterologous) baculoviruses (Goodwin et al. 1978). This work was accomplished with special 
financial support from the U.S. Forest Service. 


In cooperation with Adams, Goodwin compared the baculovirus virion morphologies of a number of 
the known baculoviruses with their host range, in order to determine if they could be separated by 
electron microscopy, e.g., wide-host-range baculoviruses (those having high mode and mean 
nucleocapsid numbers in the virion) with the narrower host range baculoviruses (lower mode and 
mean nucleocapsid numbers in the virion). This work resulted in the now accepted unicapsid and 
multicapsid baculovirus groupings (within Genus A) and the biological host range connection 
between these groupings and the more greatly differing single and multiple embedded groups 
(including the unicapsid-multiple embedded polyhedrosis of Genus A, the unicapsid-singly 
embedded granuloses of Genus B, and the non-embedded baculoviruses of Genus C). 


Goodwin developed the first serum-free insect cell culture media that supported the continuous 
cultivation of insect cell lines and, with lipidic supplementations, the first serum-free insect cell 
culture media that supported serial continuous replication cycles of a baculovirus in an insect cell 
line from the gypsy moth. These investigations made clear the dependence of virus replication on the 
nutrition and metabolism of the host cell by defining several critical nutrients that control virus 
replication and assembly events (Goodwin and Adams 1980). 


Goodwin's tissue culture media have been produced commercially, and his tissue culture research 
with other insect pathologists at Beltsville was honored with a merit-cash award for the team 
research on baculovirus cell culture replication studies. Industry and other researchers are now using 
cell lines developed by Vaughn together with cell culture media developed by Goodwin as models 
for the industrial production and study of baculoviruses in tissue cultures for several biotechnological 
and agricultural applications. 


D.E. Lynn joined the IPL in January 1981 to fill the position vacated by Goodwin when he 
transferred to the ARS Rangeland Insect Laboratory in Bozeman, MT. Lynn came to Beltsville from 
a postdoctoral position at the Insect Attractants, Behavior and Basic Biology Laboratory in 
Gainesville, FL, after graduate work at Ohio State University. His research on insect cell cultures 
continued the type of research that Goodwin had performed at the IPL. Initial success at Beltsville 
was seen with the development of cell lines from Diabrotica undecimpunctata (Lynn and 
Stoppleworth 1984). This was only the second time cells had been successfully cultured from 
Coleoptera. Cell lines from other insects followed, most notable were cell lines from gypsy moth fat 
body which have led to a probable commercial system for production of the gypsy moth nuclear 
polyhedrosis virus (LdMNPV) (Lynn et al. 1988, 1989). 


Lynn has enjoyed productive collaboration with other members of the IPL as well as many scientists 
in other laboratories at Beltsville and elsewhere. Collaboration with scientists at Gainesville, H. 
Oberlander and S.M. Ferkovich, resulted in the discovery of a new developmental hormone (Lynn 

et al. 1985) which has effects in cell culture but whose effects in the insect are still unknown. Studies 
with the spiroplasma group in IPL (K.J. Hackett, R.F. Whitcomb, and T.B. Clark) resulted in the first 
growth of two previously uncultivable spiroplasma species, the Colorado potato beetle spiroplasma 
(Hackett and Lynn 1985) and the Drosophila sex-ratio spiroplasma (Hackett et al. 1986). Research 
with scientists in the Beltsville Insect Physiology Laboratory (currently the Insect Neurobiology and 
Hormone Laboratory), M.F. Feldlaufer and W.R. Lusby, led to the first report on the production of 


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the insect molting hormone 20-hydroxyecdysone by insect cell lines (Lynn et al. 1987). A 
collaboration with A.C.F. Hung (Beneficial Insect Laboratory, currently the Bee Research 
Laboratory) led to the development of cell lines from small parasitic wasps in the genus 
Trichogramma (Lynn and Hung 1986, 1991). One of these has recently been shown by Lynn to 
undergo morphological transformation into muscle-like cells in response to treatment with insect 
molting hormone (Lynn and Hung 1991). This is the first continuous insect cell line to have such a 
developmental capacity. Lynn's primary research has been studies with NPVs in cell cultures. His 
efforts with Dougherty and Shapiro have led to a system for producing the gypsy moth NPV in cell 
cultures. 


Martin Shapiro transferred to the IPL in the fall of 1985 from the Gypsy Moth Methods Development 
Laboratory (USDA-APHIS) at Otis ANGB, MA (see below), and has continued his research studies 
on baculoviruses. The objective of his research has been to obtain information on factors affecting 
the performance of insect viruses so that viruses can be more effective in controlling insect pest 
populations. The factors being studied are: 1) virulence, 2) environmental persistence, i.e., radiation 
stability, and 3) host susceptibility. The main emphasis has been centered on the gypsy moth and its 
nuclear polyhedrosis virus (LdMNPV). 


Research on increasing viral potency has progressed through several stages. First, he identified the 
most virulent NPV isolates from North America and Asia (Shapiro et al. 1984). Second, he 
demonstrated that heterogeneity among samples within geographical isolates is a common 
phenomenon and developed a means to identify the most active samples (Shapiro and Robertson 
1991). Third, he selected for a more virulent biotype from a heterogeneous NPV population using in 
vivo methodology. While in vivo selection reduced the heterogeneity, in vitro plaquing was required 
to obtain a genetically homogeneous biotype (Shapiro et al. 1992b). The selection process and the 
improved virus biotype(s) were licensed to American Cyanamid and a U.S. Patent was issued for this 
technology on July 21, 1992. The improved virus became part of a successful in vitro production 
system, which was licensed to American Cyanamid. 


Shapiro continued and intensified research started at the APHIS Otis Methods Development Center 
at Otis ANGB, MA, on ultraviolet (UV) screens or protectants, as environmental stability is affected 
adversely by solar UV radiation. This research has been systematic and multifaceted and has 
included: 1) sunscreens for human usage (Shapiro et al. 1983); 2) insect tissues and metabolites 
(Shapiro 1984); 3) B Vitamins (Shapiro 1985); 4) dyes (Shapiro 1989; Shapiro and Robertson 1990); 
and 5) optical brighteners (Nickle and Shapiro 1992; Shapiro 1992). Research on UV inactivation 
and UV protectants has demonstrated the usefulness of several chemical structures as radiation 


protectants, indicated useful chemical structures, shed light on mechanisms of UV inactivation, and 
stimulated other scientists. 


Recently Shapiro demonstrated that certain optical brighteners (i.e., selected stilbenes) acted as 
effective UV protectants and activity enhancers for the gypsy moth NPV (Shapiro and Robertson 
1992). For the past two years, collaborators have demonstrated significant enhancement under field 
conditions, and this research has become part of an ARS-funded pilot program under R.E. Webb, 
ARS Insect Biocontrol Laboratory, Beltsville, MD). Subsequent research by Shapiro and J.J. Hamm 
(ARS, Tifton, GA) demonstrated that enhancement could occur with several viruses against the fall 
armyworm (Hamm and Shapiro 1992). This research was so attractive to American Cyanamid that a 
Cooperative Research and Development Agreement was obtained to investigate the mode of action of 
these brighteners. The use of brighteners was awarded a U.S. Patent on June 23, 1992 (Shapiro et al. 
1992a) and was licensed to both Sandoz Inc. and to American Cyanamid. 


In 1972, at an interdisciplinary conference at the Ciba Foundation in London, the field of 
spiroplasmology was launched with the description, by a Beltsville group of which R.F. Whitcomb 


304 


was a member, of a new group of helical mollicutes (Davis et al. 1972). The newly discovered 
organisms tracked the symptoms of the destructive stunt disease of corn, and were presumed to 
represent the etiological agent. The corn stunt agent was the first recognized representative of the 
spiroplasmas. Shortly after this discovery, as part of a major ARS reorganization, Whitcomb became 
a member of the IPL. Although the corn stunt spiroplasma played a pivotal role in the discovery of 
spiroplasmas and in the establishment of the genus Spiroplasma, it resisted attempts at cultivation. At 
the 1974 Bordeaux Mycoplasma Congress, Whitcomb, collaboratively with D.L. Williamson, 
announced that they had succeeded in cultivating the agent. Publication of this work (Williamson and 
Whitcomb 1975) laid the groundwork for laborious steps that culminated, 12 years later, in the 
establishment of a binomial name for the corn stunt spiroplasma (Whitcomb et al. 1986). 


In part through the work of Whitcomb (Secretary of the Subcommittee on Taxonomy of Mollicutes 
of the International Committee on Systematic Bacteriology) and colleagues, the division Tenericutes 
was created as a prokaryotic taxon equivalent in rank with the Gram-positive and Gram-negative 
bacteria, and standards were developed for descriptions of new species (Whitcomb 1979). Within 
this division, the single class Mollicutes included, among others, the families Spiroplasmataceae and 
Acholeplasmataceae. There are now more than 40 species or putative spiroplasma species. The status 
of this grouping has changed continually as new spiroplasmas have been discovered (Whitcomb et al. 
1983; Tully et al. 1986). 


These discoveries were pursued actively by an international collaborative team including scientists 
from Beltsville, National Institutes of Health (NIH), State University of New York (SUNY) Stony 
Brook, and Institut National de la Recherche Agronomique (INRA), Bordeaux, France. Spurred by 
these emerging discoveries, this group soon reported spiroplasmas from citrus, Drosophila 
(Williamson and Whitcomb 1974) and ticks (Tully et al. 1976, 1981; Stiller et al. 1981). In insects, 
mollicutes multiplied readily, and in some they were clearly pathogenic (Whitcomb et al. 1973; 
Whitcomb and Williamson 1975, 1979). The citrus and corn spiroplasmas proved to be related (Tully 
et al. 1973). After the transfer of T.B. Clark to the IPL, this field of research exploded, with Clark's 
discovery of a spiroplasma causing mortality in honey bees (Clark 1977). This was followed in rapid 
succession by Clark's discovery of spiroplasmas in a multitude of insects, including other bees, 
wasps, beetles, flies, and butterflies (Clark 1982). It was this work, and subsequent collaborative 
works of Clark, Whitcomb and Hackett (Clark and Whitcomb 1984; Hackett and Clark 1989), that 
established Spiroplasma, discovered a mere decade before at Beltsville, as perhaps the most 
abundant and diverse microbial genus on earth. The genus contains organisms that invade horse flies, 
mosquitoes, beetles, and many other pest insects. Some of the spiroplasmas proved to be 
microbiologically unique. One of these was the group VII MQ-1 strain, which produces an 
eukaryotic-like methylase and stimulates production of tumor necrosis factor, proven to have 
biomedical applications. Unfortunately, Clark died in 1984 on a field trip to Mexico. 


An entirely new approach to cultivation of fastidious mollicutes was inaugurated with Hackett and 
Lynn's (1985) use of insect cells to co-culture the Colorado potato beetle spiroplasma. This was 
followed (Hackett et al. 1986) through previously established collaborative ties, by cultivation of the 
sex-ratio spiroplasma, a transovarially transmitted male lethal organism. Work in the cultivation of 
these metabolically restricted and fastidious microbes led to insights into pathology and medical 
applications. Following cultivation of the corn stunt spiroplasms in M1D medium, J.G. Tully of the 
U.S. National Institutes of Health (NIH) and Whitcomb, pursuing leads developed in the IPL (Jones 
et al. 1977), cultured, in Whitcomb's SP-4 medium, the suckling mouse cataract spiroplasma, an 
organism originally thought to be a virus, later a spirochete, but finally revealed to be a spiroplasma. 
Koch's postulates (proof of pathogenicity; Stanier et al. 1957) were fulfilled for this spiroplasma 
(Tully et al. 1977). The M1D and SP-4 formulations have subsequently become standard media for 
cultivation of spiroplasmas and medically important mycoplasmas. For example, SP-4 medium is the 
medium of choice for isolation of the atypical pneumonia agent in man, and of a human genitourinary 


305 


mycoplasma. SP-4 is also the only medium that supports the growth of mycoplasmas believed to 
potentiate infection of the HIV virus in AIDS patients. The use of a complex medium to cultivate the 
suckling mouse cataract agent, an organism that attacks the brain of neonate mice, was followed 
(Hackett et al. 1987) by development of a completely defined medium for this very fastidious 
mollicute, and demonstration of the critical component sphingomyelin in the medium. Because of the 
high concentration of sphingomyelin in the brain, the linkage with brain pathology is explicable. This 
case has been used to illustrate the importance of nutritional studies as a window to the mechanisms 
of pathology. 


Important accomplishments were also made in the understanding of spiroplasma ecology (Hackett 
and Clark 1989). These included: 1) demonstration of the dependence of spiroplasmas on internal, 
environmentally protected, microhabitats within terrestrial arthropods, including ticks and 
holometabolous insect orders; 2) establishment of spiroplasmas in all types of insect symbioses, 
including phoresy, commensalism, parasitism, and mutualism; 3) proof that spiroplasmas invade 
insect guts, blood, and tissues, including the brain; 4) fulfillment of Koch's postulates for many plant 
and animal spiroplasmas (Stanier et al. 1957); 5) demonstration of the role of flowers and leaf 
surfaces in the dissemination of most spiroplasmas; and 6) revelation of the major association of 
spiroplasmas with a number of pest insects. 


Spiroplasmas were not the only mollicutes isolated from insects or plant surface habitats. Many 
species of nonhelical wall-less organisms also were isolated. Some of these organisms (Whitcomb 

et al. 1982; Williamson et al. 1990) proved to represent a new taxon of arthropod-associated 
mollicutes, which, paradoxically, also includes the first mollicute discovered, Mycoplasma mycoides, 
the agent of bovine contagious pleuropneumonia. The Beltsville group was closely involved in 
preparation of a comprehensive book about plant and insect mollicutes, Volume V of “The 
Mycoplasmas” (Whitcomb and Tully 1989), which was dedicated to Clark. 


Throughout these years, the mollicute team also worked on mycoplasma-like organisms (MLOs) 
causing plant disease, and on the vectors that transmit these agents. For the MLOs that are 
pathogenic to their vectors (Whitcomb and Williamson 1979), this research was a synthesis of insect 
and plant pathology. 


GYPSY MOTH METHODS DEVELOPMENT LABORATORY, OTIS ANGB, MA. By Martin 
Shapiro 


ARS maintained a research unit at the APHIS Methods Development Center at Otis ANGB, MA, for 
several years. Initially, the primary research at Otis dealt with the development of mass rearing 
technology for the gypsy moth. As a team member, Martin Shapiro worked on artificial diets. As the 
insect pathologist, he worked on development of more efficient egg-disinfection procedures, and 
improved sanitation in rearing. Rearing costs were reduced 5-fold to $12—20 per 1,000 harvested 
pupae (Bell et al. 1978, 1981). These improvements led to the establishment of mass rearing 
programs for both in vivo virus (ARS) and sterile male (APHIS) production. These rearing 
techniques represented the "state-of-the-art" and have been utilized by other laboratories. In 1977, 
each member of the ARS research team was awarded a Certificate of Appreciation "For outstanding 
adaptability and proficiency as a team member in conducting research to develop technology to rear 
sufficient numbers of gypsy moth larvae to produce the gypsy moth virus on a commercial scale". 


More simplified and efficient procedures for in vivo production of gypsy moth NPV were developed, 
culminating in a large-scale pilot plant production in 1979 (Shapiro et al. 1978, 1980, 1981; Shapiro ) 
1981, 1982; Shapiro and Bell 1981, 1982a). More than 15 million insects were infected over a 100- 

day period, and more than 50,000 acre equivalents of NPV were produced. New and immediately 

applicable information was obtained regarding factors influencing both the yield and quality of the 


306 


virus product (Shapiro and Bell 1981; Podgwaite et al. 1983). Costs were reduced from $20-30 per 
acre to $150—200 per acre equivalent or less than one-tenth of previous costs. The development of a 
practical host-larval rearing and virus production system overcame a major barrier to the use of the 
gypsy moth NPV in operational pest management systems. The virus production technology was 
subsequently transferred to USDA-APHIS and to a private company. 


Differences in the virulence of naturally occurring geographical isolates of the gypsy moth NPV from 
North America, Europe, and Asia were demonstrated. The most active isolates generally originated 
from North America; the least active isolate originated from Asia (Japan) (Shapiro et al. 1984). In a 
cooperative study, it was demonstrated that the greatest DNA homology between the North American 
standard (Hamden, CT) and other isolates occurred among North American isolates, intermediate 
homology occurred with European isolates, and no homology occurred with the Asian isolate 
(Shapiro and Dougherty 1985). Jn vivo selection of a North American isolate (Abington, MA) was 
initiated and was based upon the inherent heterogeneity of the wild-type virus population, utilizing 
time of larval death and LC,, as selectable traits. This research led to a patent (Shapiro et al. 1992a) 
and licensing to American Cyanamid of the selected NPV strain. Much emphasis was placed upon 
effective ultraviolet (UV) protectants, as environmental stability is affected adversely by solar 
radiation, especially in the UV portion of the spectrum. This research approach was multifaceted and 
has involved: 1) sunscreens for human usage (Shapiro et al. 1983); 2) insect tissues and metabolites 
(Shapiro 1984); and 3) B vitamins (Shapiro 1985). In addition, a UV-tolerant NPV biotype was 
obtained after selection (Shapiro and Bell 1984). Initial research was based upon the presumption 
that absorption in the UV-B portion of the solar spectrum was essential for good UV protection and 
excellent materials such as benzylidene sulfonic acid and uric acid were found. Subsequently, it was 
demonstrated that absorption in the UV-A portion of the spectrum was also very important and the 
effectiveness of such B vitamins as folic acid and riboflavin was shown (Shapiro 1985). In the case 
of folic acid, field efficacy was demonstrated by the U.S. Forest Service. 


Research on the gypsy moth NPV also included the use of such chemicals as boric acid to increase 
host susceptibility (Shapiro and Bell 1982b), the effect of host stage upon quality and quantity of 
NPV production (Shapiro et al. 1986), and the use of alternate hosts to produce baculoviruses 
(Shapiro et al. 1982). Research was also initiated on the entomogenous nematode, Steinernema 
carpocapsae (as Neoaplectana or S. feltiae) against gypsy moth (Poinar et al. 1981; Shapiro et al. 
1985a, 1985b). 


BIOLOGICAL CONTROL OF INSECTS RESEARCH LABORATORY, COLUMBIA, MO. By 
Arthur H. McIntosh 


In 1956, it was proposed that a research laboratory be established to conduct basic and applied 
research on the biological control (by parasitoids, predators, and pathogens) of insect pests. A 
decision was made in 1957, with the concurrence of the University of Missouri at Columbia (UMC), 
to locate the research laboratory in Columbia, MO. Factors which were important in selecting a site 
were both practical and historic: UMC had a long standing commitment to agricultural research; a 
well recognized Department of Entomology attracted high caliber scientific personnel; and modern, 
extensive library facilities were available. Construction began in 1965 and was completed in 1968. 
The new laboratory was called the Biological Control of Insects Research Laboratory (BCIRL). The 
mission of BCIRL was and is to discover, define, and verify biological control concepts and 
principles for the use of parasites, predators, and pathogens against destructive agricultural insect 
pests. 


F.R. Lawson, who was in charge of the ARS Tobacco Research Laboratory in Oxford, NC, was the 
first director of the newly established ARS laboratory. C.M. Ignoffo directed the laboratory from 


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1971 to 1989. A.H. McIntosh assumed the directorship in 1989 and continues in that capacity at 
present (1993). 


The year 1964 marked the arrival of Benjamin Puttler, a Research Entomologist, who was one of the 
first staff members of the BCIRL. The contribution to the insect pathology efforts by Puttler was his 
ability to discover and/or recognize diseases in field populations of pest insects and cooperate in 
studies of those that showed promise. He was the first to recognize the presence of the alfalfa weevil 
fungus, Zoophthora phytonomi, in the Mid-Great Plains and its potential as a factor in reducing 
alfalfa weevil populations (Puttler et al. 1978, 1980). His field observations of Nomuraea rileyi 
showed that the fungus has different levels of virulence in several of its hosts in the legume system 
(Puttler et al. 1976, 1978; Puttler and Long 1980). He also discovered potential agents for microbial 
control of the yellowstriped armyworm. 


Studies involving dissemination of nuclear polyhedrosis virus (NPV) occlusion bodies (OB) in the 
environment, importation of exotic pathogens for the control of insect pests, and incorporation of 
feeding adjuvants with viral and bacterial insecticides were conducted by D.L. Hostetter, a Research 
Entomologist at BCIRL who joined the staff in 1966. Hostetter demonstrated that Trichoplusia ni 
NPV OB were disseminated through bird feces and that entomophagous insects such as sarcophagid 
flies which fed on diseased larvae also served as disseminators of virus (Hostetter and Biever 1970). 
The recovered virus was virulent for the target pest. Such studies were important in understanding 
the epizootics of virus diseases in the environment. Hostetter was also successful in demonstrating 
control of the imported cabbageworm with a granulosis virus imported from Canada (Hostetter et al. 
1973). He demonstrated the effectiveness of Bacillus thuringiensis (Bt) against bagworm which 
resulted in expanding the label of this microbial pesticide for this insect. It was shown that the 
insecticidal activity of commercial preparations of Bt and a viral insecticide of corn earworm could 
be extended by the addition of adjuvants to formulations (Hostetter et al. 1975, 1982). Hostetter also 
showed that the use of a fungicide (Kocide 101 WP) at recommended application rates had no 
deleterious effect on the entomopathogenic fungus of alfalfa weevil or the occurrence of epizootics in 
an endemic area. These findings are important to management techniques and decisions for the 
control of insect pests. 


In more recent studies, two new multiple enveloped nuclear polyhedrosis viruses (IMNPV) have been 
researched. An MNPV isolated from the yellowstriped armyworm in Missouri was shown to be host 
specific (Hostetter et al. 1990). An MNPV isolated from the celery looper (Anagrapha [=Syngrapha] 
falcifera) in Missouri was shown to infect more than 31 species of Lepidoptera (Hostetter and Puttler 
1991). The MNPV from celery looper is equally effective against larvae of corn earworm and 
tobacco budworm as contrasted to the Autographa californica MNPV (AcMNPV) which has a low 
virulence for corn earworm. The celery looper baculovirus (AfMNPV) was the first baculovirus ever 
patented (and it is a potential biological insecticide for commercial production and licensing because 
of its wide host range and effectiveness against the Heliothis/Helicoverpa complex and other 
lepidopteran larvae. This example of technology transfer between ARS and private industry has 
resulted in efforts to commercialize this virus by Sandoz Inc. and biosys®. 


In 1968, K.D. Biever initiated studies to characterize the development of the nuclear polyhedrosis 
virus of the cabbage looper under programmed temperature regimes (Biever and Hostetter 1971, 
1985). These data provided a reliable method of predicting and characterizing natural epizootics and 


determining expected larval mortality patterns when virus is used to control field populations of 
cabbage looper. 


Biever, in cooperation with Hostetter, developed a biological pest control program for lepidopterous 
pests of wine and juice grapes (Biever and Hostetter 1975, 1989). This program eliminated the use of 
chemical insecticides by successfully substituting the judicious use of Bt, which is non-toxic to 


308 


humans and leaves no harmful residue. This program offers great potential for wide acceptance and 
implementation given present trends in pest control. 


Biever carried out studies during 1974-1976 that established that imported cabbageworm stressed by 
temperature manipulation and/or inadequate diet moisture would exhibit overt infection and succumb 
to a subacute granulosis virus (Biever and Wilkinson 1978). Results of these studies highlighted the 
importance of environmental stressors in the recovery or infection processes for larvae exposed to 
virus. 


A pest management system for control of the diamondback moth, the cabbage looper, and the 
imported cabbageworm in commercial cabbage production was developed by Biever (Biever and 
Hostetter 1978; Davis et al. 1985). A workable system was provided for growers which eliminated or 
minimized the use of chemical insecticides and reduced production costs through use of a microbial 
insecticide and a population monitoring system. Several commercial growers currently use this 
system for cabbage production. 


In 1979 and 1980, Biever implemented laboratory and field cage studies that demonstrated that a 
predator, the spined soldier bug, could mechanically transmit an entomopathogenic virus to cabbage 
looper larvae via leaf surfaces and initiate epizootics that provided high levels of population 
suppression (Biever et al. 1982). These findings have opened a new area of research effort and 
opportunity involving the use of predators and parasites to vector specific insect pathogens in crop 
systems. Subsequently, Biever conducted studies that established the importance of placement of 
insect virus on the plants in relation to the specific feeding behavior of the target insect. He 
demonstrated that selective placement of the virus significantly increased its effectiveness and 
provided residual control. 


Upon arrival at BCIRL in 1971, C.M. Ignoffo continued his research in the field of insect pathology 
and microbial control. Ignoffo was instrumental in the precedent development and registration of the 
world's first viral pesticide and in the formulation of protocols for registering candidate microbial 
pesticides (Ignoffo 1973a and b, 1979). The concept and initial research establishing the feasibility of 
virus production, safety to non-target organisms and field effectiveness was initiated by Ignoffo at 
USDA-ARS at Brownsville, TX (see below) and completed while he was with International Minerals 
and Chemical Corporation (IMC) at Wasco, CA. His research on the interrelationships between this 
registered virus ("Heliothis SNPV"), its Heliothis/Helicoverpa complex hosts, and the environment 
continues to the present date. Ignoffo's more recent research has focused on explaining the 
mechanism(s) of sunlight inactivation of microbial insecticides with specific reference to the 
"Heliothis SNPV", an entomopathogenic fungus (Nomuraea rileyi) and the bacterium, Bt. He was 
one of a few early investigators who advocated the importance of sunlight-UV inactivation of field- 
applied microbial insecticides and is the co-inventor of a patent describing a natural polyflavonoid 
(while at IMC at Libertyville, IL) that was used in commercial formulations as an UV-protectant for 
both chemical and microbial pesticides. He has utilized a number of UV protectants to successfully 
stabilize microbial insecticides in the field and has made important contributions to the 
understanding of the mechanism(s) of inactivation of microbial pathogens by sunlight (Ignoffo and 
Batzer 1971; Ignoffo et al. 1974, 1977c, 1989b, 1991; Ignoffo and Garcia 1978b). 


Ignoffo, as the leader of an interdisciplinary research at BCIRL, evaluated the status and role of 
biological control agents such as parasites, predators, and pathogens in a soybean-model-ecosystem. 
Information from such studies provided knowledge on pest/natural enemy interactions as well as 
provided a model system for recommendations to soybean growers in Missouri and the Midwest. 
Furthermore, the basic and applied knowledge garnered from these studies was useful in the control 
and suppression of insect pests and the reduced use of chemical insecticides, increasing the return on 
investment to soybean growers (Ignoffo et al. 1976c; Ignoffo 1980). 


309 


lgnoffo also conducted basic and applied studies on the entomopathogenic fungus WN. rileyi and 
demonstrated that it was a promising and safe microbial agent. An Experimental Use Permit (EUP), 
approved by U.S.-EPA for the use of N. rileyi as a mycoinsecticide, was granted to Abbott 
Laboratories. The EUP permitted industrial production of N. rileyi and its distribution to independent 
researchers conducting field tests in the southern U.S. Further studies were conducted by industry, 
university, and federal scientists to test the efficacy of N. rileyi as a mycoinsecticide. Results 
indicated N. rileyi can be effectively used as a prophylactic microbial control agent but has limited 
use unless directed at early instar larvae. Other studies involving N. rileyi included: strain 
identification, propagation, virulence of geographical isolates, storage stability, chemical sensitivity, 
environmental fate and dispersal, safety, formulation and timing of field application (Ignoffo et al. 
1975a and b, 1976a, b, c and d, 1977a, b and c, 1978, 1979, 1982a and c, 1983, 1985, 1989a; Puttler 
et al. 1976; Garcia and Ignoffo 1977, 1978, 1979; Ignoffo and Garcia 1978a and b, 1985, 1987, 1991; 
Ignoffo 1981; Ignoffo and Boucias 1992). 


Ignoffo conducted a series of studies on the possible role of fungal enzymes in the infection process 
(El-Sayed et al. 1991, 1992a and b; Gupta et al. 1991, 1992; Ignoffo and Garcia 1991). Most 
investigators used enzymes (proteases, lipases, chitinases) expressed by fungal mycelia to study the 
host-penetration-infection process. Ignoffo advocated concentrating on conidia (from WN. rileyi) 
because they are primarily and intimately involved in penetration of the integument that eventually 
leads to the host's death (Ignoffo 1981). 


Working in collaboration with M.H. Greenstone, an Arthropod Ecologist hired at BCIRL in 1982, 
Ignoffo also documented the host-range of a congener of N. rileyi, N. atypicola, which prior to that 
time had been known only from a few spiders (Greenstone et al. 1987). 


Some of the earliest studies with a newly isolated mosquito bacterium (Bacillus thuringiensis 
israelensis) also were conducted at the BCIRL in collaboration with industrial and other USDA 
scientists (Ignoffo et al. 1980, 1981a and b, 1982b). 


The arrival of A.H. McIntosh, a Research Microbiologist, in 1979 at BCIRL provided the much 
needed disciplines of insect cell culture and virology not previously available at the Laboratory. Jn 
vitro systems provide a means of conducting experiments at the cellular level that would be difficult 
or impossible to accomplish in vivo. Effort was concentrated on the worldwide important agronomic 
insect pest complex of Heliothis/Helicoverpa and its homologous single nuclear polyhedrosis virus 
(HzSNPV). 


McIntosh established the first insect cell lines from several major insect pests: tobacco budworm 
(McIntosh et al. 1981), Helicoverpa armigera (McIntosh et al. 1983), diamondback moth (Quhou 
et al. 1983), yellowstriped armyworm, corn earworm, imported cabbageworm, and Heliothis 
subflexa. These lines are routinely used in research projects at the BCIRL and have been requested 
both nationally and internationally by scientists for use in molecular biology, virology, genetics, 
biochemistry and physiology. McIntosh was the first to successfully apply the isoelectric focusing 
(IEF) technique for the identification of insect cell lines (McIntosh and Ignoffo 1983, 1989). Cell 
lines showed distinct patterns of their own, but could be closely correlated with their host or origin. 


MclIntosh demonstrated the feasibility of producing occlusion bodies of HzSNPV in corn earworm 

and tobacco budworm cell lines and clones thereof (McIntosh and Ignoffo 1981; Lenz et al. 1991). 

Some clones produced significantly greater numbers of occlusion bodies (OB) and extracellular virus : 
(ECV) than parental lines. The advantages of the in vitro system for virus production are that it : 
provides a cleaner system, free from adventitious agents, one that is easily monitored, and could 

provide more continuity and flexibility during commercial production. The disadvantage of in vitro 

production lies in its greater cost. However, this problem is being solved with the development of 


310 | 


serum-free media in which the expensive component, fetal bovine serum (FBS), has been excluded. 
HzSNPV has been produced in corn earworm lines grown in serum-free media with greater 
production of both OB and ECV than observed in cells grown in medium containing serum 
(McIntosh et al. 1991). Since insect cells can be produced in large-scale suspension cultures, the 
major impediment for commercial production of HZSNPV in vitro is the low market demand. In a 
study of viral infectivity, it was discovered that virions released from OB by alkali treatment could be 
made more infectious for cell cultures by treatment with a proteolytic enzyme, proteinase K 
(McIntosh and Ignoffo 1988). 


McIntosh et al. (1984), in one of the few complete studies of this kind, showed that in vitro 
specificity paralleled in vivo specificity and that MNPV tended to have a broader host range than 
SNPV. He demonstrated that AfMNPYV has a wide host range in vitro and produced the highest ECV 
titer in the H. subflexa cell line (McIntosh 1991). Jn vitro systems can serve as a rapid means for 
establishing the host range of viral isolates from nature. 


In 1980, with the arrival of T.A. Coudron, a Research Chemist, research was initiated that resulted in 
the discovery of biochemical pathways leading to basic information on virulence and infectivity of 
entomopathogenic fungi. Coudron discovered a complex enzyme profile used by entomopathogenic 
fungi for the degradation of chitin. The information provided significant detail about characterization 
of the enzymes involved in the infectivity of these organisms (Coudron et al. 1984). A two-enzyme 
system was shown to be secreted by entomopathogenic fungi for the degradation of insect chitin 
which was comprised of multiple forms of the enzymes in the system. Coudron also demonstrated a 
correlation of the chitinolytic activity with virulence where a pronounced increase in chitinolytic 
activity appeared in entomopathogenic strains prior to and at the time of infection (El-Sayed et al. 
1989). A new semi-liquid medium and techniques for rearing entomopathogenic fungi were also 
developed that were ideal for the extraction of proteolytic enzymes produced by most Hyphomycetes 
(Coudron et al. 1985). 


In 1985, W.C. Rice, a Research Microbiologist, initiated studies to map and characterize the genome 
of HzSNPV and to identify site(s) and genes controlling desirable traits so as to develop techniques 
for manipulating these genes for enhanced effectiveness of the virus. Rice sequenced the Xho I F 
DNA fragment (6,964 base pairs) of the HZSNPV. He found a 738 base pair open reading frame (orf) 
coding for the polyhedrin gene that was translated into a 246 amino acid polypeptide. DNA sequence 
analysis of the Xho I F fragment revealed the presence of 44 orf's. Ten orf's whose molecular weights 
were 10,000 daltons or greater were translated into polypeptides and used to search the National 
Biomedical Research Foundation (NBRF) protein data base. Other than polyhedrin, only orf-4067 
was homologous to a family of proteins, whose members belong to the kinase gene family. The 
presence of a putative kinase gene in the sequence of the baculovirus DNA has led to the use of the 
kinase assay as a direct biochemical marker. 


Serial passage studies of isolate Vhl in tissue culture cells performed by Rice resulted in the 
generation of an assortment of restriction endonuclease variants which fit into a number of discrete 
classes. Viral genomic changes were detected which were consistent with DNA insertions and/or 
deletions (McIntosh et al. 1987). Representatives of each class were bioassayed in corn earworm 
larvae and extrapolated LC,, values revealed an 800-fold difference in larval infectivity, indicating 
that possibly genes involved in virulence were disrupted (Rice et al. 1989). 


RANGELAND INSECT CONTROL RESEARCH, BOZEMAN, MT. By Douglas A. Streett 
In 1961, the Grain and Forage Insects Branch, Entomology Research Division, ARS, under the 


direction of R.G. Dahms, established a biological control of grasshoppers research project. J.E. 


311 


Henry was hired by Frank Cowan to initiate this project at the Rangeland Insect Laboratory at 
Bozeman, MT. 


Historically, attempts to control grasshoppers and locusts with fungi and bacteria produced some 
encouraging results, but most attempts had little or no effect on grasshopper population densities. 
Several gregarines, an undescribed neogregarine, an amoeba (Malameba locustae) and a 
microsporidan (Nosema locustae) had been reported in grasshoppers. While not highly virulent, M. 
locustae was sufficiently detrimental to laboratory colonies of grasshoppers that it was necessary to 
develop therapeutic measures for disease control (Henry 1968; Henry and Oma 1975). 


Field surveys of grasshoppers were conducted to determine the prevalence of known grasshopper 
pathogens and to isolate previously unknown pathogens. Two new species of microsporida were 
found and described — Nosema acridophagus (Henry 1967, 1969a) and N. cuneatum (Henry 1971b); 
and the first entomopoxvirus in Orthoptera was isolated from the migratory grasshopper (Henry and 
Jutila 1966; Henry et al. 1969). A crystalline array virus was also isolated from field-collected 
twostriped grasshopper. It represented the first isolation of an RNA virus infectious to grasshoppers 
and it appears to be one of the smallest viruses isolated from any living system (Jutila et al. 1970; 
Henry 1973; Henry and Oma 1973). Two new entomopoxviruses were also isolated from 
grasshoppers, and a cooperative study was initiated with W.H.R. Langridge of the Boyce Thompson 
Institute at Cornell University to do structural protein and DNA studies (Langridge and Henry 1981; 
Langridge et al. 1983). 


Financial and physical limitations made it necessary to select one organism for investigation as a 
potential grasshopper microbial control agent. Nosema locustae was selected on the basis of 
virulence, host range, potential for mass production and prolonged storage, suitable viability in the 
habitat of the host, low cost application techniques, and potential for registration as a microbial 
insecticide. Like most microsporida in their respective hosts, NV. Jocustae was not highly virulent. If 
applied when the predominant stages were third instars, N. Jocustae caused about 50% density 
reduction of various species within four weeks postapplication and 30-50% infection among 
survivors (Henry 1971a; Henry et al. 1973; Henry and Oma 1974a). In addition, infections result in 
significant reductions in fecundity among the survivors. The host range of N. locustae includes 58 
species of grasshoppers, a species of cricket, and a pigmy grasshopper (Henry 1969b). Most species 
of grasshoppers and some species of crickets appear to be susceptible. Nosema locustae can be mass- 
produced with relative ease (Henry 1978); however, some difficulty has been experienced in storage 
of spores (Henry and Oma 1974b). 


Studies of natural epizootics indicated that N. Jocustae should reduce both the extent and frequency 
of grasshopper outbreaks on rangelands, providing applications were made early in the season against 
economic densities and before serious damage occurred (Henry 1972). Henry (1978) reported on 
application techniques for N. /ocustae and potential for registration as a microbial insecticide. 


In 1975, a large-scale pilot test on 37,312 hectares of rangeland was initiated. Nosema locustae was 
applied by aircraft at two rates and compared with a standard rangeland insecticide treatment of 
malathion, and with no treatment. The high dosage caused significant reductions in grasshopper 
densities during the season of treatment. A panzootic among grasshoppers caused by the fungus 
Entomophaga grylli occurred early in the second season and apparently reduced the prevalence of N. 
locustae. Nevertheless, the high rate caused significant reductions, and the low rate appeared to cause 
slight but not significant reductions in grasshopper densities during the two subsequent seasons. 
Parasitism of grasshoppers by entomophagous flies and nematodes decreased sharply in malathion- 


treated plots, but tended to increase in N. /ocustae-treated and untreated plots (Henry and Onsager 
1982). 


a12 





Nosema locustae became the first protozoan to be registered as a microbial insecticide in the U.S. in 
1978. Another study was conducted to increase efficiency of production of spores of N. locustae. The 
differential grasshopper is a hardy species for laboratory rearing with a higher survival potential that 
results in greater spore production (Henry 1985). Oma and Hewitt (1984) reported that the females of 
this grasshopper infected with N. /ocustae consumed less food than uninfected females, but there was 
no significant difference in food consumption by infected and uninfected males. 


Cooperative projects were initiated with scientists from Argentina; Carlos Lange and Georgina Luna 
came to Bozeman for training in insect pathology. Experimental infections were conducted with N. 
locustae, N. acridophagus, and N. cuneatum in 12 species of Argentine acridids in order to determine 
their susceptibility. All 12 species were susceptible to NV. /ocustae (Luna et al. 1981). Lange returned 
to Bozeman in 1985 for further studies. A new species of microsporida, Perezia dichroplusae, was 
described from the Argentine grasshopper Dichroplus elongatus (Lange 1987). 


D.A. Streett came to the Rangeland Insect Laboratory in 1980 as a post-doctoral scientist. The 
incidence of infection and transmission of an undescribed microsporidan in field populations of two 
species of grasshoppers were studied (Streett and Henry 1984). Because the original description of N. 
cuneatum was done with light microscopy, an ultrastructural investigation was undertaken and 
reported by Streett and Henry (1987). 


During 1981—1983, studies funded by U.S.-AID were conducted on the susceptibility of West 
African grasshoppers to N. Jocustae. Application of spores on wheat bran to field plots in Cape 
Verde and Mauritania resulted in infection of most species of Acrididae. Based on the taxonomic 
diversity of these species, it was likely that most, if not all, West African grasshoppers were 
susceptible to infection by N. /ocustae (Henry et al. 1985a). Pathogenic microorganisms isolated 
from West African grasshoppers included entomopoxviruses, protozoa, fungi, and a rickettsia (Henry 
et al. 1985b, 1986). The DNA from six orthopteran entomopoxviruses were characterized. 
Restriction enzyme patterns for each of the viruses was found to be unique (Streett et al. 1986). 
Cross-infectivity studies of these six viruses to various species of grasshoppers showed that some 
isolates appeared to infect grasshoppers of different taxa, whereas some isolates seemed to be 
restricted to particular taxonomic groups of grasshoppers (Oma and Henry 1986). 


The Grasshopper Integrated Pest Management (GHIPM) Project was organized in 1987 in response 
to record-setting grasshopper infestations that blanketed millions of acres of U.S. rangeland in the 
mid-1980s. Initiated as a pilot study, the project was designed to develop and integrate grasshopper 
control strategies into a total system for use by managers of public and private rangelands. The 
GHIPM Project was a co-operative effort managed by the APHIS in association with other USDA 
agencies and the U.S. Department of Interior, Environmental Protection Agency, state universities, 
and rancher associations. The mission of the Pathology Group at the Rangeland Insect Laboratory 
was to further develop known pathogens as control agents and look for possible unknown pathogens 
which could be developed as control agents. A viral DNA probe was developed to detect early 
entomopoxvirus infections in grasshoppers (Streett and McGuire 1988). 


In November, 1987, Henry retired and Streett was hired to head up the pathology group. Henry is still 
active in on-going grasshopper control projects in Africa and the development of Vairimorpha sp. as 
a control agent for the Mormon cricket. 


JAPANESE BEETLE LABORATORY, MOORESTOWN, NJ. By Michael G. Klein 


See Wooster, OH. See also Beltsville, MD, for early history. 


313 


PLANT PROTECTION RESEARCH UNIT, ITHACA, NY. By Richard A. Humber 


A program and laboratory for study of fungal entomopathogens for use in biological control was 
established and built at Orono, ME, in 1972 and moved to the Cornell University campus in 1978. 
Personnel were initially housed in the Boyce Thompson Institute and, in 1989, moved to the U.S. 
Plant, Soil, and Nutrition Laboratory. Before moving to Ithaca, the program was focused on an 
international cooperative effort involving the Rothamsted Experimental Station and the Pasteur 
Institute to develop techniques to mass produce and germinate resting spores of entomophthoralean 
fungi (now known as Conidiobolus thromboides and C. obscurus) for use against aphids (Soper et al. 
1975). 


A research collection of entomopathogenic fungal cultures started by Richard S. Soper and taken 
over in 1976 by Richard A. Humber evolved into one of the largest collections of microbial 
germplasm in ARS, and the world's foremost collection of entomopathogenic fungi. As of 1991, the 
ARS Collection of Entomopathogenic Fungal Cultures (ARSEF) comprised more than 3,200 isolates 
from more than 250 fungal species that are distributed on request. The catalog of the ARSEF culture 
collection (Humber 1992) is widely distributed. Staff at ARSEF provide identification of fungal 
pathogens without charge, and are internationally recognized for research on the biology and 
systematics of these fungi (e.g., Humber 1981, 1989; Roberts and Humber 1984), providing critical 
support worldwide for basic and applied programs involving fungal entomopathogens. 


From 1980 to 1991, a program was established on the biology, epizootiology, and practical use of 
entomophthoralean fungi in the Entomophaga grylli species complex infectious to grasshoppers and 
locusts. The program led to the successful field establishment of an Australian isolate against 
grasshoppers in North Dakota under the auspices of a large-scale IPM demonstration project on 
grasshopper control (GHIPM). This project yielded the unexpected discovery that sun-basking by 
diseased grasshoppers may raise their body temperatures enough to cure infections by microbial 
pathogens (Carruthers et al. 1988b). 


Early studies on grasshopper fungi led to the realization that many fungi in the Entomophthorales 
(and also many ascomycete and deuteromycete pathogens of invertebrates) routinely stop sporulating 
when desiccated but again produce infective spores when rehydrated. A process for drying mycelial 
mats of Zoophthora radicans (for use initially against spruce budworm) was developed and patented 
(McCabe and Soper 1985). Dried mycelia can be milled, stored, and rehydrated upon application to 
produce fresh infective spores in the field. Now, dried mycelia techniques are used successfully with 
diverse fungal entomopathogens. It is the predominant methodology worldwide for the practical 
application of fungi to control invertebrate pests. 


Classical biological control introductions involving fungal entomopathogens are relatively rare, but 
the ARS Plant Protection Research Unit (PPRU) played a key role, in cooperation with the 
Commonwealth Scientific and Industrial Research Organisation (CSIRO), in successfully introducing 
a pathogen of spotted alfalfa aphid (SAA) (Milner and Soper 1980; Milner et al. 1982). The PPRU 
screened strains of Zoophthora radicans from the ARSEF culture collection for activity against SAA 
and guided the introduction of an Israeli strain of the pathogen into northeastern Australia. At the 
time, SAA was causing severe damage to Australian alfalfa and was the focus of a major pest control 
program within CSIRO. 


In 1910-11, a Japanese pathogen of gypsy moth was introduced to six sites around Boston (Speare 
and Colley 1912) with no apparent successful establishment. This entomophthoralean fungus, which 
was later described as Entomophaga maimaiga (Soper et al. 1988), was nearly forgotten until Scper 
collected it in Japan in 1984 and began new studies of its potential to control gypsy moth (G22 
Shimazu and Soper 1986). A fungus causing widely publicized mortality of gypsy moth larvae across 


314 


the northeastern U.S. during 1989 and 1990 proved to be E. maimaiga. Because the fungus causing 
the panzootic was biochemically indistinguishable from Japanese strains of E. maimaiga, and 
because no modern introductions of E. maimaiga were made in the affected regions, it was inferred 
that the massive mortality of gypsy moth must have been caused by the fungus introduced 80 years 
earlier by Speare and Colley (Hajek et al. 1990). This case provides a rare and outstanding instance 
where it may be possible to follow the long-term survival and dispersal of an introduced insect 
pathogen. 


Beauveria bassiana, the most common fungal entomopathogen, is distributed worldwide. The 
pathogen has been used widely to control Colorado potato beetle (CPB) in the former Soviet Union 
as well as various lepidopteran pests of both corn and forests in the People's Republic of China. 
However, it has not been commercialized or used widely in the U.S. or Europe. The PPRU 
coordinated the first substantive pilot field testing of B. bassiana in the U.S. against CPB in several 
potato-growing states (Hajek et al. 1987; Anderson et al. 1988). 


During the 1980s, it became increasingly clear that many pathogens of insects had shown a poor 
track record for practical use in biological control programs because of insufficient understanding of 
how these disease agents operate under field conditions. An appreciation of the value of 
epizootiological studies (Onstad and Carruthers 1990) and modelling of host-pathogen interactions 
became a high priority in many invertebrate pathology laboratories. Leading work in these subjects 
was undertaken by the PPRU on B. bassiana against CPB and entomophthoralean pathogens against 
grasshoppers. These studies yielded a modular computer program called "Simulation Environment 
for Research Biologists (SERB)" (Larkin et al. 1988) that facilitated the rapid construction of useful 
simulation models by persons having no specialized background. A simulation modelling approach 
has been instrumental in evaluating and guiding epizootiological studies on grasshopper pathogenic 
fungi (Carruthers et al. 1988a). 


HORTICULTURAL INSECTS RESEARCH LABORATORY, WOOSTER, OH. By Michael G. 
Klein 


Following the transfer of the Insect Pathology Unit from Moorestown, NJ, to Beltsville, MD, in 
1954, research on pathogens of the Japanese beetle ceased for many years. W.E. Fleming (1968) 
reviewed the many published and unpublished reports on efforts to control the Japanese beetle with 
protozoa, fungi, nematodes, bacteria, and rickettsia from 1920 (shortly after the discovery of the 
Japanese beetle near Moorestown, NJ) until 1964. This excellent summary has made a wealth of 
information available to insect pathology students and researchers. 


Most of the information during the past 40 years on pathogens of the Japanese beetle has centered on 
the use of Bacillus popilliae, the causal agent of milky disease. Ladd and McCabe (1966) followed 
up the earlier milky disease colonization program by surveying the state of New Jersey. They found 
the milky disease organism active at colonization sites, and movement of the bacteria into 
uninoculated areas. Schwartz and Townshend (1968) reported that B. popilliae caused an increase in 
hemocytes in diseased larvae early in the infection process, but no alteration in the coagulation of the 
hemolymph. Further work by P.H. Schwartz (Schwartz and Sharpe 1970) demonstrated that spores of 
B. popilliae produced in vitro lacked infectivity when fed to Japanese beetle larvae. Problems in 
obtaining in vitro sporulation, and lack of infectivity of the spores that were produced, led to the 
cessation of efforts by USDA in this area. 


The Japanese Beetle Laboratory was moved from Moorestown, NJ, to Wooster, OH, in September 
1971. M.G. Klein et al. (1976) prepared a bibliography of the milky disease bacteria. Nearly one 
third of the 250 citations dealt with bacterial physiology as a result of the efforts to produce B. 
popilliae on artificial media. Since that time, over 80 additional papers on milky disease bacteria 


1 


have been published. Fleming and Ladd (1979) updated information for the homeowner and other 
turf grass managers on the use of milky disease for suppression of Japanese beetle populations. 


During the past ten years, Klein (1981, 1982, 1986, 1988, 1989, 1992; Klein and Jackson 1992) has 
focused attention on the prospects of using milky disease bacteria against scarab larvae throughout 
the world, and examined the problems that prevent more successful use of the bacteria. Recently the 
misidentification and lack of infectivity in bacteria produced on artificial media was demonstrated 
(Stahly and Klein 1992). The use of other bacteria (Klein and Jackson 1992) and other 
microorganisms against scarab and non-scarab pests of turf have also been explored (Klein 1982, 
1988, 1989; Kaya et al. 1992, 1993; Cranshaw and Klein 1994). Klein (1990, 1993) also examined 
the past use of entomopathogenic nematodes against soil-inhabiting pests, identified the obstacles to 
greater acceptance of these organisms in the suppression of pest populations, and demonstrated that 
they could be used as inoculative agents (Klein and Georgis 1992). 


The mission of the Japanese Beetle Laboratory has been expanded to cover other horticultural pest 
insects, and to develop new application technologies. Insect pathology will remain an important 
component. 


U.S. VEGETABLE LABORATORY, CHARLESTON, SC. By Kent D. Elsey and James M. Schalk 


In 1967, F.P. Cuthbert, Research Entomologist at the U.S. Vegetable Laboratory, Charleston, SC, 
discovered a mermithid nematode parasitizing Diabrotica spp. in the Charleston area (Cuthbert 
1968). This nematode was described by Poinar (1968) and named Filipjevimermis leipsandra. 
Subsequent research on this nematode at Charleston involved mass rearing (Creighton and 
Fassuliotis 1982), temperature relations (Elsey 1989, 1991), seasonal fluctuations in the field, and 
infectivity in the laboratory (Creighton and Fassuliotis 1980). Attempts to augment natural 
populations in corn plantings against Diabrotica larvae were hindered by problems associated with 
soil moisture and temperature interactions. 


Several entomopathogenic fungi attack sweetpotato weevil, including Beauveria bassiana, Isaria sp., 
and Metarhizium anisopliae. Both B. bassiana and M. anisopliae were shown to have some potential 
for management of the weevil (Chalfant et al. 1990). Entomopathogenic nematodes that attack the 
weevil include Steinernema sp. and Heterohabditis heliothidis. Unidentified heterorhabditid species 
and other rhabditid nematodes have been isolated from sweetpotato weevil in southern Florida. A 
heterorhabditid nematode, ‘HP88’ strain, was more effective than a steinernematid nematode and 


chemical insecticide in suppressing weevil populations and protecting roots from damage (Chalfant 
et al. 1990). 


In another study, interaction between larvae of the banded cucumber beetle, a resistant sweetpotato 
cultivar, a susceptible sweetpotato clone and an arthropod nematode, H. heliothidis (South Carolina 
strain) were evaluated. No significant interactions between the nematode and cultivar type were 
observed, and adult emergence was drastically reduced when second instars were exposed to the 
nematode in both cultivars. When second instars were exposed to the nematode, the duration of the 
adult eclosion period was reduced because of the lower number of insects emerging. The nematode 
had no effect on emergence or duration of eclosion period of third instars. Higher levels of parasitism 
in younger larvae can be attributed to their longer development time which increases their exposure 
to the parasite. The mobility of third instars may be greater than younger larvae allowing them to 
evade the parasite. They may also be less susceptible to the parasite. The duration of the eclosion 
period was negatively correlated with adult weight (Schalk and Creighton 1989). 


Efficacy of Steinernema carpocapsae (All Strain) against banded cucumber beetle larvae was 
investigated (Schalk unpublished). Late first instar and early second instar larvae were confined in 


316 


crispers in the laboratory and exposed to the nematode at the rate of 1/1.2 g of soil (blasting sand). 
Emergence of adults in the untreated controls were 80% while 0.5% emergence was observed in the 
parasite treatment. Mean adult weight was 14.6 mg for the controls and 8.2 mg for the parasite 
treatment. 


NORTHERN GRAIN INSECTS RESEARCH LABORATORY, BROOKINGS, SD. By Jan J. 
Jackson 


G.R. Sutter initiated the insect pathology/biological control program at the Northern Grain Insects 
Research Laboratory (NGIRL), Brookings, SD, in 1965. During the late 1960s, several cutworm 
species and the armyworm were serious pests of small grains and corn in the Northern Plains. 
Calkins and Sutter (1972) developed techniques to assist surveys of parasitism and diseases in field 
populations. To support pathological studies, rearing methods were developed for the army cutworm 
(Sutter and Miller 1972) and the pale western cutworm (Sutter et al. 1972). Rearing methods were 
also developed for the parasitoids Glyptapanteles militaris using the armyworm (Calkins and Sutter 
1976) and Copidosoma bakeri using the army cutworm. The histopathology of rickettsia-like 
organisms in four species of carabid beetles (Sutter and Kirk 1968) and a poxvirus (Sutter 1972), a 
non-occluded virus (Sutter 1973), and a granulosis virus (Jackson and Sutter 1985) in the army 
cutworm were subsequently reported. McCarthy et al. (1975) further characterized the poxvirus of 
the army cutworm. 


Entomological research at the NGIRL shifted to an emphasis on corn rootworms in the early 1970s. 
Southern corn rootworm larvae and adults of the western and northern corn rootworms were found to 
be insensitive to treatments with Bacillus thuringiensis and B. popilliae (Sutter 1969). Field surveys 
for parasites and diseases of corn rootworm adults in South Dakota yielded no parasites and few 
pathogens. Collections of adults from other Corn Belt states also yielded few parasites or pathogens 
but the incidence of natural enemies increased with collections from states along the southern 
boundary of the rootworm population distribution. Gregarine protozoans were frequently found in 
field collected adults but the incidence was low most years. Gregarine infections in laboratory 
colonies were often extensive and when combined with nutritional stress, high adult mortality was 
observed. Gregarine morphology, development, pathogenicity, and cultural methods to reduce 
gregarine infections in laboratory colonies of rootworms were described (Brooks and Jackson 1990). 
In 1983, studies on insect-parasitic nematodes for larval corn rootworm control were initiated. 
Filipjevimermis leipsandra and several steinernematids were found to be pathogenic for rootworm 
larvae and pupae. Jackson and Brooks (1989) described the pathogenicity and immune response of 
four strains of Steinernema carpocapsae. The susceptibility of larval stages and development in 
rootworm larvae and pupae was described (Jackson 1985). Laboratory and field evaluations have 
been encouraging but improved efficacy is needed. 


COTTON INSECTS RESEARCH LABORATORY, BROWNSVILLE, TX. By Carlo M. Ignoffo, 
Howard R. Bullock, Leslie C. Lewis, and Clayton C. Beegle 


In 1959, investigations in insect pathogens/microbial control began in the Rio Grande Valley at 
Brownsville, TX, with the employment of C.M. Ignoffo. Ignoffo focused his basic and applied 
research on the use of entomopathogens to control cabbage looper on truck crops, and 
Heliothis/Helicoverpa spp. and other lepidopterans infesting cotton. Ignoffo conducted early research 
on the effects of Bacillus thuringiensis (Bt) on pink bollworm larvae which included the effects of 
temperature and humidity on mortality (Ignoffo 1962a and b). Later field cage tests were conducted 
with Bt for the control of the pink bollworm (Ignoffo and Graham 1967). Earlier attempts by 
investigators to continuously rear the cabbage looper generally were unsuccessful because of 
contaminants many thought to be inherent occult viruses. This was proven false when methods were 
developed to mass rear the cabbage looper using aseptic techniques and a newly developed semi- 


317 


synthetic diet (Ignoffo 1963a). In further studies, Ignoffo determined the sensitivity of Bt to various 
antimicrobial substances commonly used in insect semi-artificial diets that might influence its 
activity (Ignoffo 1963b). These studies demonstrated the undesirable effects of some of these 
materials on Bt and the consequent influence on apparent activity in bioassays. Their potential to 
control Bt contaminants in mass rearing was also demonstrated. Later, Ignoffo and Dutky (1963) 
demonstrated the antimicrobial effects of sodium hypochlorite on the viability and infectivity of Bt 
and Beauveria spores and the nuclear polyhedrosis virus (NPV) of the cabbage looper. Ignoffo 
(1964a) also studied the effects of temperature and water on the viability and virulence of Bt spores. 
The above studies were important to the later development of mass rearing, production and 
standardization systems for the Heliothis/Helicoverpa and cabbage looper NPV. 


Ignoffo's efficacy studies with microbial control agents were conducted using Bt for the control of 
the cotton leafworm, a pest of cotton in the southern U.S. (Ignoffo et al. 1964). These studies led to 
more intensive studies on the development of baculoviruses and other entomopathogens as insect 
control agents. 


The previous studies by Ignoffo (1963a) on mass rearing the cabbage looper served as a basis for 
developing mass production methods for the singly embedded NPV infectious to this species. The 
studies on antimicrobial agents previously conducted also were incorporated into the production 
schemes in order to reduce extraneous microbial contaminants. Ignoffo (1964c) published the first 
mass production method for a baculovirus utilizing the newly developed semi-artificial diet. This was 
the first publication on insect virus production in which live host plants were not used for the host 
insect used for production. Ignoffo (1964b) described bioassay procedures also utilizing the new 
semi-artificial diets which provided methods for determining virulence of the produced virus as a 
basis for standardization of production lots. The methods for cabbage looper and corn earworm 
rearing and virus production were later consolidated into a methodology publication (Ignoffo 1966d). 


Ignoffo's earlier work led to an intensive study in 1961 of a nuclear polyhedrosis virus infectious to 
the Heliothis/Helicoverpa complex as a microbial control agent (Ignoffo 1973a). This 
bollworm/budworm complex was selected because of the worldwide distribution of species which 
are severely destructive to many economic plants (e.g., cotton, corn, tobacco, tomatoes, vegetable 
crops, seed crops). The virus used in these studies and eventual commercialization was first isolated 
from diseased Heliothis/Helicoverpa larvae attacking cotton in the Rio Grande Valley of Texas 
(Ignoffo 1965a). Annual costs to control Heliothis/Helicoverpa were extremely high. Before 
commercialization of the virus, its effectiveness against field populations on several crops, 
amenability to continuous large-scale production under laboratory conditions, nucleic acid 
composition, and its effects on man, other animals and plants were determined (Estes and Ignoffo 
1965; Ignoffo 1965a, b, and c; Ignoffo and Heimpel 1965; Ignoffo et al. 1965). These studies 
indicated further development was warranted. 


Steps toward the eventual commercialization began conceptually in 1961 and continued through 
early 1965 at the Brownsville laboratory (Ignoffo 1965a, b, and c; Ignoffo et al. 1965). From 1962 
until 1964, basic research on insect host mass production, virus production, activity and 
standardization was conducted which set parameters for pilot plant and full production phases. Field 
tests on corn, cotton, and grain sorghum were conducted with the virus resulting from the above 
studies (Ignoffo 1965d; Ignoffo et al. 1965). Safety tests (Ignoffo and Heimpel 1965) were also 
initiated in anticipation of submitting a registration package to the U.S. Food and Drug 
Administration (FDA). 


The rearing techniques developed in this program made it possible to produce large numbers of 
Helicoverpa zea larvae, and resultant virus production throughout the year. The virus was produced 
continually from May through August 1963, providing large amounts of standardized material for. 


318 


field testing as described above. Approximately 250,000 larvae were produced during this period or 
enough to treat 2,000—8,000 acres of cotton. The methods and procedures developed during this time 
were then adopted to pilot production and production phases. 


Other studies conducted in support of this project included the effects of temperature on H. zea 
larvae exposed to sublethal doses of the virus (Ignoffo 1966b). Because it was possible that the virus 
might be used in tank mixes with chemical insecticides and adjuvants, the influence of these 
materials on the virus was determined (Ignoffo and Montoya 1966) as well as the possible use of dust 
formulations of virus (Montoya and Ignoffo 1966). Ignoffo and Garcia (1966) also determined the 
influence of pH on the activity of inclusion bodies which could be of major concern in certain parts 
of the United States having highly alkaline water. Ignoffo (1966a and c) determined the influence of 
larval age on susceptibility of both the bollworm and tobacco budworm. In 1965, Ignoffo was 
employed by Bioform Corporation, later acquired by International Minerals Corporation, to develop 
the Heliothis/Helicoverpa virus into a commercial product. The “Heliothis SNPV" was registered in 
1970. FDA granted a temporary exemption from the requirement of a tolerance. It was the first 
baculovirus registered and mass produced for commercial use. Commercial products based on this 
exemption were initially made available by International Minerals Corporation, Libertyville, IL, and 
Nutrilite Products Inc., Buena Vista, CA. In the late 1970s and early 1980s, Sandoz Inc., San Diego, 
CA, produced and marketed the virus under the trade name of “Elcar”™., Although still registered, 
the virus is not now produced commercially or sold for control of the bollworm/budworm complex in 
the U.S. More cost competitive chemical pesticides (i.e., pyrethroids) introduced during the late 
1970s and early 1980s eliminated the market. 


H.R. Bullock became a member of the insect pathology investigations at Brownsville, Texas in 1965 
after having a post doctoral appointment at the ARS Insect Pathology Laboratory in Beltsville, MD. 
Bullock and Dulmage (1969) conducted tests with Bt for control of the pink bollworm, which had 
recently also become a serious pest of cotton in Arizona and California. Their laboratory tests 
indicated larvae were highly susceptible and they therefore conducted field cage studies to determine 
if the microbial had potential for pink bollworm control. They found that rosetted blooms and mines 
were reduced, and number of bolls was higher, and concluded that Bt should be investigated under 
field conditions for pink bollworm control. Bullock (1967) also conducted research on the 
persistence of the “Heliothis SNPV" on cotton foliage and found that most activity was lost after one 
day. He proposed losses may be due to ultraviolet (UV) light and/or mechanical loss. Bullock et al. 
(1970a) conducted further studies on inactivation of "Heliothis SNPV" by determining the influence 
of monochromatic UV on activity. Wavelengths of 257 nm and 307.5 nm inactivated the virus. 
Visible and infrared may also have had an effect. Bullock also evaluated encapsulated "Heliothis 
SNPV" polyhedra obtained from the National Cash Register Company (Dayton, OH). Such 
encapsulated polyhedra had increased persistence under field conditions. These studies further 
helped in the understanding of factors which may affect virus persistence under field conditions, one 
of the major impediments to the development of viruses as microbial control agents. 


Bullock et al. (1969) found that high concentrations of formaldehyde would reduce cytoplasmic 
polyhedrosis virus (CPV) contamination of pink bollworm eggs but the effect also was dependent 
upon the level of contamination present. They concluded that surface contamination of eggs was an 
important means of virus transmission. They also noted the eggs were not dechorionated and thus 
timing of the treatment was not critical. In further investigations, Bullock et al. (1970b) noted the 
adverse effects of CPV infection on pink bollworm such as delayed development, larval mortality, 
reduced longevity, and fecundity of diseased moths. However, egg hatch and mating were not 
affected. Bullock (1972) determined the therapeutic value of heat treatments for a cytoplasmic 
polyhedrosis virus infectious to tobacco budworm larvae. He also noted teratological effects incurred 
with increasing temperatures. These two treatments provided several methods of managing CPV in 
insect colonies. 


319 


H.T. Dulmage became a staff member in the mid-1960s and conducted research on Bacillus 
thuringiensis (Bt). In the early development of Bt, the spore was thought to be the sole source of 
insecticidal activity leading to emphasis on spore production in commercial fermentations. This led 
to the acceptance of spore count as a method of standardization. However, Dulmage and Rhodes 
(1971), and others, demonstrated that there was no reliable relationship between spore-count and 
potency. When it was determined that the 6-endotoxin was the primary insecticidal component, 
conferences were convened to develop a protocol to standardize Bt products on an international unit 
(IU) basis (Dulmage 1973a and b). A preparation of Bt subspecies thuringiensis (designated E-61) 
was adopted as the international standard and was assigned a potency of 1000 IU/mg (Dulmage et al. 
1971; Dulmage 1973a). Meanwhile, industry had adopted a more potent strain of Bt from subspecies 
kurstaki. Thus, the U.S. Environmental Protection Agency requested that a standard be produced and 
adopted of the same serotype as that being commercially produced (subspecies kurstaki). In 1972, 
HD-1-S-1971 was adopted as the Primary U.S. Reference Standard with an assigned potency of 
18,000 IU/mg (Dulmage 1973a and b). Today, all preparations of Bt produced in the U.S. for use 
against lepidopterous larvae are standardized against HD-1-S-1971 or its successor HD-1-S-1980. 
Standard HD-1-S-1980 has a potency of 16,000 IU/mg. Some companies also use an international 
HD-1 standard which was initially standardized against HD-1-S-1971. Dulmage also contributed to 
the protocol used to standardize Bt subspecies israelensis (McLaughlin et al. 1984). 


Dulmage (1970a) isolated a Bt subspecies kurstaki (first identified as subspecies alesti; see de Barjac 
and Lamille 1970) from diseased pink bollworm larvae. This isolate, designated HD-1 (HD 

= Howard Dulmage) by Dulmage, proved to be from 20 to 200 times more potent than the isolates 
used in existing commercial products (Dulmage et al. 1978). In 1970, Abbott Laboratories entered 
the market with Dipel®, the first commercial preparation based on HD-1. Dulmage accumulated 
isolates of Bt world wide to study diversity within and between isolates. To accomplish this task, he 
formed the International Cooperative Program on the Spectrum of Activity of Bt (BtICP). 


BtICP was designed to find more potent isolates of Bt to use in the control of insect pests. This 
program was also developed to learn more about the insecticidal, serological, and bacteriological 
characteristics of the toxins produced by different Bt isolates. 


Dulmage contributed substantially to developing insect-diet-based assays to standardize Bt products 
(Dulmage et al. 1971, 1976; Burgerjon and Dulmage 1977; Beegle et al. 1982). His assay was the 
first to propose the use of a standardized insect and a standardized procedure to determine [Us of 
products. Many of the present day assays are modifications of the technique. 


Dulmage was a member of a team that determined that isolates within subspecies of Bt could be 
distinguished by crystal serology (Krywienczyk et al. 1978, 1981). He also contributed significantly 
to early work with fermentation media to produce spore/crystal powders with maximum yields of 
activity (Dulmage 1970b, 1971; Dulmage et al. 1970; Salama et al. 1983). He was also a member of 
many research teams that investigated insecticide activity of many isolates of Bt and B. sphaericus 
against many insects (Davidson et al. 1984; Dulmage and Aizawa 1982; Trottier et al. 1988); 
identified previously unknown isolates (Dulmage and de Barjac 1973; Rodriguez-Padilla et al. 1990); 
identified factors affecting insecticidal activity (Lacey et al. 1978); and conducted initial research on 
the genetics and protein chemistry of B. thuringiensis (Gonzalez et al. 1981; Yamamoto et al. 1983). 


C.C. Beegle joined the laboratory in 1976 through a Cooperative Agreement with Texas A&M 
University in order to expand the Bt research program; he became an ARS scientist in 1977. The first 
standardized assay developed to determine potency of Bt products specified the incorporation of 
aureomycin with larval diet to eliminate vegetative stages of Bt. Research by Beegle et al. (1981b), 
however, showed that LC., values of Bt, when neonatal larvae of three insect species were used in 
bioassays, were not significantly different when antibiotic was omitted from the insect diet. 


320 


Conversely, when the antibiotic chlortetracycline hydrochloride was incorporated into the bioassay 
diet of 4-day-old larvae, the LC,, values were increased from 2 to 67 times. Beegle et al. (1986) 
developed the assay defining the use of subspecies kurstaki (HD-1-S-1980) as the reference standard 
used in the U.S. Also, it was found that the use of a standard will not in all cases correct for 
differences in assay techniques (Beegle 1990); thus, a new assay was jointly developed by ARS and 
U. S. commercial firms to determine potencies of lepidopterous-active preparations (Beegle et al. 
1991). Even though sophisticated, highly repeatable, standardized bioassays have been developed, 
researchers cannot duplicate the impact of the environment in laboratory settings, i.e., field 
performance dosages cannot always be extrapolated from laboratory data (Beegle et al. 1982). 


Beegle was actively involved in research on production of exotoxins by certain isolates (Mohd-Salleh 
et al. 1980), use of new methods such as crystal serology to determine that some mosquito-active 
isolates of Bt have mixed crystals (Krywienzcyk et al. 1981), identification of isolates with superior 
potencies (Beegle 1983; Beegle and Yamamoto 1983), and use of fermentation to increase potencies 
of Bt isolates (Beegle et al. 1991). He also determined the half-life of insecticidal activity on cotton 
leaves was between 15 and 2 days (Beegle et al. 1981a). 


KNIPLING-BUSHLAND U.S. LIVESTOCK INSECTS RESEARCH LABORATORY, 
KERRVILLE, TX. By Richard E. Gingrich and Kevin B. Temeyer 


Research with arthropod pathogens at the Livestock Insects Laboratory (now the Knipling-Bushland 
U.S. Livestock Insects Research Laboratory), Kerrville, TX, began in 1964 with investigations by 
R.E. Gingrich on the use of Bacillus thuringiensis for control of horn, stable, and house flies. The 
objective was to develop microbial feed additives that would pass through the bovine intestine and 
control larvae that normally develop in contact with the feces. After demonstrating that currently 
available commercial Bt products were active when fed to cattle it was learned that the B-exotoxin 
was the toxic agent (Gingrich 1965; Gingrich and Eschle 1966, 1971; Gingrich and Haufler 1978). 
Applications by incorporation in slow release boluses deposited in the rumen and by incorporation in 
daily rations of range cubes were successful for controlling larvae in feces and, in case of the latter 
application, for reducing adult horn fly populations on range cattle (Gingrich 1984). The safety of B- 
exotoxin applied in this manner was demonstrated when cows produced normal offspring after 
sustained ingestion of B-exotoxin during pregnancy. In further studies, it was determined that the 
soluble exotoxins produced by Bt are heterogeneous in chemical character, spectrum of susceptible 
host insects, and mammalian toxicity. The potential of Bt for control of biting lice was also 
demonstrated (Hoffmann and Gingrich 1968; Gingrich et al. 1974). 


Gingrich participated in the International Cooperative Program (BtICP), initiated by another ARS 
scientist, H.T. Dulmage, to study the spectrum of activity of Bt (Dulmage et al. 1981). Using horn fly 
larvae, and the "goat louse", Bovicola sp., he demonstrated the persistence of exotoxins in the 
experimental samples distributed to cooperators for bioassay and presented further evidence of the 
heterogeneity among them. 


This research continued through 1982 when K.B. Temeyer was hired to continue Bt research begun 
by Gingrich, and to assess the potential development, using recombinant DNA technology, of Bt as a 
microbial agent against biting flies. In addition to the cooperative screening work with Dulmage, 
work with B-exotoxin was being conducted in Kerrville. Previous work had clearly demonstrated the 
toxic effect of B-exotoxin to fly larvae. In order to assess the toxicity of components other than B- 
exotoxin, it was necessary to develop an assay capable of determining how much B-exotoxin was 
present in a particular preparation of Bt. This was accomplished through use of high performance 
liquid chromatography (HPLC) (Oehler et al. 1982). Further research demonstrated that B-exotoxin 
from B. thuringiensis subspecies morrisoni was differentially toxic to male and female mice, with 


o21 


males being more sensitive than females (Haufler and Kunz 1985). B-exotoxin was also shown to 
exhibit toxic and teratological effects to larvae of the oriental rat flea (Maciejewska et al. 1988). 


Careful analysis of the literature, together with thorough review of the horn fly larvae bioassay 
results obtained with various strains of Bt appeared to suggest that the crystal protein of B. 
thuringiensis subspecies israelensis (Bti) might be larvicidal to horn flies, but that the Dulmage 
preparations were not stable under prolonged storage. Bioassay of freshly grown Bti preparations 
confirmed that subspecies israelensis was larvicidal to horn flies. Biochemical separation of 
endospores, crystal protein, and low-density particulate matter coupled with bioassay revealed that 
the larvicidal activity resided in the crystal protein (6-endotoxin) and low-density particulate 
fractions. The toxicological properties of the two fractions were distinct, suggesting the presence of 
at least two different Bti toxins possessing larvicidal activity to horn flies. Both toxins appeared at 
sporulation, and were not produced in the presence of streptomycin, an inhibitor of protein synthesis, 
suggesting that Bti produced two sporulation-specific proteins which were larvicidal to horn flies 
(Temeyer 1984). This was the first report of Bt crystal protein toxicity to muscid flies and the first 
report of the presence of a second Dipteran-active toxic protein produced by Bti. The possibility that 
one of the Bti toxins might be related to B-exotoxin was considered. Bacillus thuringiensis 
subspecies israelensis was not known to produce B-exotoxin, an ATP analog exhibting strong 
larvicidal activity to flies and produced by a number of Bt strains during vegetative growth (see 
Sebesta et al. 1981). Further analysis, together with HPLC confirmed that neither Bti preparations 
contained B-exotoxin (Temeyer 1990b). These results suggested that there were at least three distinct 
toxins which might form the basis for development of a Bti-derived control methodology for biting 
flies through the use of recombinant DNA technology. Interestingly, preparations of B. sphaericus 
known to exhibit high toxicity to mosquito larvae failed to demonstrate toxicity to horn fly larvae by 
bioassay (Temeyer unpublished). It is not known whether B. sphaericus toxins are ineffective to horn 
fly larvae, or whether they are inactivated by components of the bovine fecal medium. 


Identification of specific toxic proteins was difficult due to problems in obtaining biochemical 
separation of the multiple crystal proteins present in subspecies israelensis (Chilcott et al. 1983; 
Pfannenstiel et al. 1984; Thomas and Ellar 1984). It seemed that a more convenient approach might 
be to clone the individual crystal protein components separately into a non-toxic genetic background 
such as B. subtilis, and screen recombinants expressing the various Bti crystal proteins separately and 
in combinations to assess individual toxicity of proteins, and the potential synergistic interactions 
which might occur. Construction of organisms containing recombinant DNA from another species 
required approval by a Recombinant Advisory Committee (RAC) or an institutional biosafety 
committee (IBC) in accordance with the "NIH Guidelines", whereas construction of homologous 
recombinants of Bt did not require advance approval. But there was no well characterized cloning 
system available for Bt. There was considerable confusion within the agency and elsewhere at the 
time as to what body had the authority and regulatory jurisdiction to conduct biosafety reviews. This 
situation resulted in considerable delay in commencement of the planned experiments. The ARS 
Southern Plains Area had no IBC and only one laboratory then conducting recombinant DNA 
research. Approval to construct recombinant microorganisms containing Bti toxin genes was granted 
by the ARS Beltsville Area IBC in 1986. However, by that time, the key personnel at Kerrville were 
heavily engaged in research to develop a recombinant vaccine for cattle grubs (Hypoderma spp.). 


There were a number of problems encountered in attempts to develop a homologous cloning system 
for B. thuringiensis. These included instability of recombinant DNA in Bacillus spp., the lack of 
homologous cloning vectors, and the lack of reliable methods for generating protoplasts for 
transformation (Chang and Cohen 1979), and then regenerating cell walls for the transcipient 
protoplasts. In addition, bioassays were extremely cumbersome, as well as problematic due to 
variability in bovine fecal matter resulting in occasional high mortality in control groups. This 
condition presented a strong disincentive to laborious preparation of small amounts of test material 


oe2 


a eens 


knowing that subsequent bioassays could use all of the available material without providing any 
useable data. Therefore, it was important to determine if simple modifications of the horn fly larval 
medium or bioassay procedure could increase reliability of bioassays. 


As a first approach to development of a semi-defined horn fly larval medium to replace the bovine 
fecal medium used in bioassay, a series of supplementation experiments were performed to determine 
the permissible osmotic parameters and to test the effects of supplementation with simple nutritional 
additives. Initially, sucrose was chosen as a test supplement for determination of permissible osmotic 
parameters, as it was thought unlikely to be toxic or even be taken up by the larvae. Thus, it probably 
would function as an inert solute in the bioassay system. Surprisingly, all concentrations of sucrose 
tested resulted in death of the larvae, as did many other carbohydrates. It was noted, however, that 
the larvae frequently migrated out of the fecal medium prior to death, and that, in some cases, gas 
evolution was apparent in the larval (fecal) medium, suggesting fermentation was taking place. 
Addition of streptomycin and monitoring of fecal medium pH versus time following carbohydrate 
supplementation confirmed that fermentation and consequent wide swings in the supplemented fecal 
medium pH appeared to be responsible for larval death (Temeyer 1990a) rather than direct toxicity of 
sugars as had been previously suggested for similar systems (Galun and Fraenkel 1957). It was also 
found that lipids appeared to be nutritionally limiting factors in horn fly larval nutrition, and 
supplementation with cholesterol, inositol, corn oil, or egg yolk resulted in production of heavier 
larvae and pupae, and increased survival to adulthood (Temeyer unpublished). Routine 
supplementation of bovine fecal medium with cholesterol, inositol, egg yolk, corn oil, or a 
combination of these, did not interfere with bioassays of preparations containing one or both of the 
two Bti toxins (Temeyer unpublished). It is interesting to note other strains of Bt have also been 
shown to possess similar toxicity to horn fly larvae as has subspecies israelensis (Temeyer 
unpublished). One of these, strain CAT-44 of B. thuringiensis "var. fluffiensis", obtained its name in 
a somewhat novel manner. P.A.W. Martin (Beltsville) had been attempting to determine the 
ecological niche occupied by Bt, and isolated strains of Bt from nearly everywhere she had looked. 
One day a visiting friend remarked, "Your lab smells like my cat's feet!". Just for fun, Martin made a 
paw imprint on a petri plate containing Bt-selective agar, and a number of colonies developed, 
including a strain with previously unknown characteristics. When she was talking with a reporter for 
a news article and related the story of how the strain was isolated, the reporter asked for the strain 
name. Martin replied that according to usual procedures strains are named after the source of 
discovery (place or person), she supposed that this strain should be named “fluffiensis" since the 
name of the cat was “Fluffy”. The name stuck, though it has not been published in scientific 
literature. 


Cloning experiments generally produce transcipient populations consisting of several thousand to 
several million potential recombinants. Screening such a large number of potential recombinants by 
bioassay was clearly not feasible. Alternatively, development of monoclonal antibodies was believed 
to offer a method for screening recombinant bacteria for production of Bti presumptive toxins which 
could then be subject to bioassay after selection of high expression recombinant clones. Therefore, a 
series of hybridomas secreting monoclonal antibodies specific for various component crystal proteins 
of Bt were constructed (Temeyer et al. 1986; Temeyer unpublished). U.S. Patent No. 4,945,057 
(Temeyer et al. 1990) was granted covering development and use of hybridomas and their 
monoclonal antibodies. 


Production of Bt protoplasts was determined to be unreliable by routine methods, and early 
experiments indicated that Bt cultures varied in sensitivity to lysozyme, with lysozyme-sensitive 
cultures developing resistance to lysozyme with the growth phase. Alternative methods using a 
commercially available N-acetylmuramidase or simple autolytic digestion improved the removal of 
Bt cell walls for production of protoplasts or cell-free lysates (Temeyer 1987). Unfortunately, the 


B25 


difficulty in regenerating the cell walls after complete removal has not yet been overcome, making 
protoplast transformation an, as yet, unreliable method for genetic exchange in B. thuringiensis. 


Instability of recombinant DNA in Bacillus species has been a frequently encountered problem. It is 
generally believed that the instability is a result of a combination of properties of the available 
cloning vectors and uncharacterized recombination pathways in Bacillus spp. Progress has been 
made in molecular characterization of potential mechanisms of recombination for different cloning 
vectors in Bacillus spp. (Temeyer and Chapman 1987; Hopkins et al. 1990; Temeyer et al. 1991). In 
addition, new cloning vectors are being developed which appear to exhibit improved stability in 
Bacillus spp. 


Additional experiments conducted with Tom Benoit (ARS, College Station, TX) verified that there 
was no cross-resistance to Bti in bioassays using fly strains with known resistance to pyrethroid or 
organophosphate pesticides (Temeyer and Benoit unpublished). As of November 1991, several of the 
Bti crystal protein genes have been cloned in Escherichia coli at the Kerrville laboratory. Reporter 
gene constructs are being developed to evaluate expression of unknown genes in alternate genetic 
backgrounds, as well as new cloning vehicles for Gram-positive bacteria with specific improvements 
in plasmid structure. 


HONEY BEE RESEARCH, WESLACO, TX. By William T. Wilson 


In 1985, W.T. Wilson of the Honey Bee Disease Investigations Laboratory, Laramie, WY, moved to 
the ARS Subtropical Agricultural Research Laboratory at Weslaco, TX, to continue studies on the 
honey bee. 


A rare internal protozoan (Malpighamoeba mellificae) was discovered in honey bee colonies in the 
southcentral U.S. that were experiencing adult bee mortality and severe population loss (Wilson and 
Collins 1992). With the arrival of the Africanized honey bee in south Texas in the autumn of 1990, a 
portion of the Weslaco bee research program was directed towards the diseases and parasites of this 
more defensive bee. Current studies are directed towards determining whether bees of African 
ancestry (Africanized) are more resistant to Acarapis woodi, Varroa jacobsoni and Nosema apis than 
bees of European ancestry. In 1988, A.M. Collins was appointed Research Leader of the Honey Bee 
Research Unit at Weslaco. In 1992, construction started on a new building to house the research staff 
and facilities. 


BEE BIOLOGY AND SYSTEMATICS LABORATORY, LOGAN, UT. By John D. Vandenberg 


The Bee Culture Laboratory at Logan, UT, was established in 1947 under the direction of F. Todd. In 
1973 the unit was named the Bee Biology and Systematics Laboratory. 


Insect pathology research at the laboratory concentrated on chalkbrood in the alfalfa leafcutting bee, 
but related studies of fungus infections of other bees have also been reported. Much of the work on 
leafcutting bee chalkbrood has been done cooperatively in the last 15 years. Specific Cooperative 
Research Agreements for this research, funded by ARS, were established with W.P. Stephen (Oregon 
State University), N.N. Youssef (Utah State University), D.F. Mayer (Washington State University), 
and L.P. Kish (until 1988) and C.R. Baird (University of Idaho). Additional cooperation and support 
has been provided throughout this period by the Northwest Alfalfa Seed Growers Association. 


Significant research accomplishments are many, and include the first record of chalkbrood in North 
America (Baker and Torchio 1968). Studies of fungi associated with the alkali bee and other bees 
(Batra and Bohart 1969; Batra et al. 1973) and studies of chalkbrood in the "blue orchard bee", 
Osmia lignaria propinqua (Youssef et al. 1985; Rust and Torchio 1991) are the only studies of 


324 


pathogens of these bees. Other accomplishments of laboratory scientists and specific cooperators 
constitute the history of research on chalkbrood in the alfalfa leafcutting bee. 


The alfalfa leafcutting bee is a commercially important pollinator of alfalfa in western North 
America. Bee populations are maintained near alfalfa fields in nest shelters filled with wooden, 
styrofoam or paper nest materials with drilled holes. Female bees construct a linear series of leaf- 
lined cells within the tunnels. Each cell is filled with pollen and nectar before an egg is laid. The bees 
overwinter as mature larvae (prepupae) and emerge as adults in early summer. Chalkbrood was first 
reported from commercial alfalfa leafcutting bee populations in 1974. Since then it has spread 
throughout most areas of bee cultivation. Larval mortality due to this disease can exceed 50% in 
some populations. 


Fichter et al. (1981) developed a laboratory rearing system for alfalfa leafcutting bee larvae which 
facilitated a series of studies on chalkbrood etiology and pathogenesis. Initially, a viral etiology 
followed by secondary fungus invasion was suggested for this mortality. However, Vandenberg and 
Stephen (1982) clearly showed Ascosphaera aggregata to be the causative agent of chalkbrood in the 
alfalfa leafcutting bee. Vandenberg et al. (1980) and Stephen et al. (1981) demonstrated pertinent 
aspects of chalkbrood epizootiology. As healthy adults first emerge from their nests, they are 
sometimes forced to chew through or around a sibling chalkbrood cadaver. In so doing, these adults 
can become covered with spores. Spores on adult females contaminate the pollen provisions of their 
offspring and thus spread the disease to the next generation. Bee population management techniques 
designed to minimize exposure of newly-emerging adults to chalkbrood cadavers result in lower 
disease prevalence. 


Vandenberg and Stephen (1983a, 1984) and McManus and Youssef (1984) demonstrated the 
pathogenesis, reproduction and sporulation of chalkbrood. Spores must be ingested by larvae and 
then germinate in the gut. The pH within the midgut is near neutral, but the redox potential is quite 
low. Extensive multiplication occurs within the hemocoel before death. Certain color changes 
characterize chalkbrood within a few days after death. A pink or tan patch develops initially, usually 
visible in the abdomen. Within a day after death the cadaver is uniformly brown or gray. Fungi in 
cadavers destined not to sporulate remain tan colored as they dehydrate. The mycelia in the process 
of sporulation within cadavers usually turn light gray or white prior to development followed by 
pigmentation of black spore cysts beneath the host cuticle. Sporulation is usually complete within 
1-2 weeks after death. 


Other Ascosphaera species are capable of infecting the alfalfa leafcutting bee. Vandenberg and 
Stephen (1983b) showed that although the alfalfa leafcutting bee is susceptible to infection by A. apis 
and A. proliperda, the pathology is distinctly different. Youssef et al. (1984) detailed infection of the 
alfalfa leafcutting bee by A. proliperda. 


Stephen and Fichter (1990a and b) successfully selected for leafcutting bee resistance to chalkbrood. 
After appropriate backcrosses, they concluded that resistance was probably polygenic in their 
selected lines. Consequently, resistance would likely be quickly swamped by feral or managed bees if 
resistant bees were introduced for pollination purposes. Resistance can be maintained, however, in 
isolated populations subject to continued selection pressure. 


In a series of studies, Maghrabi and Kish (1985a and b, 1986, 1987a and b) used morphology, 
cytology, and isozyme electrophoresis to examine the complex relationships among species of 
Ascosphaerales. Their study of 52 A. aggregata isolates from throughout the western U.S. (Maghrabi 
and Kish 1987b) revealed considerable uniformity in morphology and electrophoretic patterns. These 
authors raised legitimate questions concerning the specific and generic status of these fungi 
(Maghrabi and Kish 1987a; Kish et al. 1988). Because 4. aggregata sporulates in some cadavers and 


325 


not in others, it is presumed to be heterothallic, but necessary definitive studies (starting with single 
spore isolates) have not been conducted. (Ascosphaera apis, the causative agent of chalkbrood in the 
honey bee, is known to be heterothallic). However, McManus and Youssef (1991) recently reported a 
method for in vitro sporulation of this fastidious fungus. Consequently, studies of basic fungus 
biology and genetics may now be possible. 


Most recently, Vandenberg (1992a) developed a quantitative laboratory bioassay system. Larvae are 
most susceptible when inoculated at 1-3 days of age, and less susceptible at 5 days of age. LDsos 
were between 100 and 200 spores per larva, and probit regression slopes were near 10. Both average 
time to death and the weight of sporulated cadavers were inversely correlated with dose. However, 
the proportion of cadavers sporulating was highest at intermediate doses and lower at both high and 
low doses. Adults that survived inoculation as larvae exhibited no sublethal effects as judged by size 
and sex ratio. 


A large number of bees used for commercial alfalfa pollination in the United States are purchased 
from Canada because chalkbrood is not common there. Vandenberg (1992b) tested the hypothesis 
that these bees are more susceptible to chalkbrood because of their previous lack of exposure to the 
disease, but he found no difference in susceptibility between U.S. and Canadian bees. Beekeepers 
can therefore use bees from either source without incurring increased risk of chalkbrood in their bee 
populations. Further studies of the roles of bee nutrition and abiotic factors in chalkbrood 
susceptibility are underway. 


Kish (1980) developed a technique for germination of high percentages of A. aggregata spores in 
vitro. This method was an essential tool for later studies of sporicides and chalkbrood control 
methods. After extensive screening of potential sporicides, Stephen et al. (1982) identified a few 
halogen compounds (including sodium hypochlorite) as having the best potential for incorporation 
into bee management schemes. Kish (1983) demonstrated the efficacy of high temperature treatments 
in killing spores, and Kish and Panlasigui (1985) determined the efficacy of a series of preservatives 
as potential sporicides. 


Separation of the overwintering bees within their cocoons from nest materials followed by nest 
material decontamination are essential steps in prophylactic disease management. Both cocoons and 
nest materials may be effectively treated by dipping in hypochlorite solutions (Mayer et al. 1988). 
Alternatively, nest materials may be treated with high temperatures (Kish 1983). 


Youssef and McManus (1985) and Youssef and Brindley (1989) tested the efficacy of three 
fungicides — captan, botran, and carbendazim — by incorporating each fungicide with fungus spores 
in the provisions of laboratory-reared larvae. Their findings were similar for all three fungicides: low 
doses resulted in reduced chalkbrood incidence, and higher doses caused larval mortality. Fichter and 
Stephen (1987) tested nine fungicides at a series of doses, also using laboratory-reared bee larvae. 
Both benomy] and carbendazim effectively controlled chalkbrood and did not harm developing 
larvae. In contrast to field studies by Parker (1984, 1985, 1987, 1988; see below), captan did not 
significantly reduce chalkbrood and caused mortality or extended developmental times for bee 

larvae. 


In a series of field studies using thrice-weekly dust applications in nest shelters, Parker (1984, 1985, 
1987, 1988) demonstrated the efficacy of captan for chalkbrood control. Other fungicides tested — 
benomyl, botran, and carbendazim — were not effective. In contrast to the laboratory findings of 
Fichter and Stephen (1987) and Youssef and McManus (1985), Parker noted no effect of captan on 
larval survival. Both Fichter and Stephen (1987) and Parker (1984, 1985, 1987) noted an increased 
frequency of non-sporulating forms of chalkbrood with increasing fungicide dose. This phenomenon 
could help control the spread of chalkbrood to the next generation of bees. Mayer et al. (1990) 


326 


applied six fungicides in fields of leaf sources used by bees for nest construction. None was 
consistently effective, compared to controls, in reducing chalkbrood; however, captan was not 
included in their test. Clearly, additional studies are needed before any of these fungicides can be 
recommended or approved for field use. 


In summary, research on chalkbrood in the alfalfa leafcutting bee conducted by scientists and 
cooperators of the ARS Bee Biology and Systematics Laboratory has provided a solid foundation for 
bee management and disease control. Research continues on several fronts, including studies of bee 
genetics, chalkbrood susceptibility, fungus molecular biology, and prophylactic and chemical control. 


YAKIMA AGRICULTURAL RESEARCH LABORATORY, YAKIMA, WA. By K. Duane Biever 


From 1953 to 1988, several entomologists at the Yakima Agricultural Research Laboratory have 
evaluated microbials as part of their ongoing research programs on fruit and vegetable insect pests. 


During the 1960s, J.F. Howell evaluated the nematode Steinernema carpocapsae against the codling 
moth. Applications of the nematode were directed at the overwintering populations and were 
ineffective. In the late 1970s, Howell (1979) developed a new method for storing and collecting the 
nematode. This was a spin-off of a program evaluating the nematode against the bertha armyworm 
and the "spotted cutworm", Xestia (as Amathes) c-nigrum. Foliar treatments were not effective for 
the bertha armyworm and provided 40-50% mortality of the cutworm. In 1980 and 1981, H.H. Toba 
evaluated two species of nematodes (S. carpocapsae [as feltiae] and S. glaseri) for activity against 
the sugarbeet wireworm (SBWW) and the Colorado potato beetle (CPB) (Toba et al. 1983). They 
demonstrated that inundative soil applications of S. carpocapsae in field cages reduced larval 
populations of CPB and SBWW, 71 and 29%, respectively. 


Howell evaluated the codling moth granulosis virus (SAN 4061, Sandoz Inc., San Diego, CA) in 
apple orchards in 1981 and 1982. The virus caused larval mortalities of 72 to 82% for the first 
generation and 32 to 74% for the second generation. 


Researchers at the Yakima Laboratory participated in a 3-year pilot test evaluating the efficacy of 
foliar applications of Beauveria bassiana for control of the CPB (Hajek et al. 1987). R.L. Chauvin 
supervised the project in 1983 and K.D. Biever, reassigned from the ARS Laboratory in Columbia, 
MO, in early 1984, assumed leadership of the project through its completion in 1985. Foliar 
treatments reduced first generation CPB populations by 65%, suggesting that B. bassiana could be an 
important component of an IPM system. In 1987, as part of a program on developing an insect 
management system for potatoes, Biever evaluated several rates of a strain of Bacillus thuringiensis 
specific to the CPB (M-ONE™, Mycogen Corporation) under an Experimental Use Permit. Two 
applications, at rates from | to 4 quarts per acre (22,500 IU/mg), against the first generation reduced 
larval populations from 17 to 55%. 


STORED PRODUCTS LABORATORY, MADISON, WI. By Wendell E. Burkholder 


Insect pathology/microbial control research began at the Stored Products Laboratory at Madison, WI, 
in the late 1950s. During that time, research with several dermestid species of the genus Trogoderma 
was impeded by epizootics of the neogregarine protozoan Mattesia trogodermae. The pathogen 
caused severe epizootics in the laboratory and was suspected of suppressing field populations of 
Trogoderma species in grain bins and in food processing and storage facilities. In the process of 
developing insect cultures free of the pathogen, it was observed that the diseased insects fluoresced a 
bright yellow-green under 366 my ultraviolet light (Burkholder and Dicke 1964). The UV technique 
is a convenient tool assisting in both insect rearing and research to monitor for the presence of 
Mattesia spores. 


Ave | 


Subsequent studies were conducted of the pathogenicity and development of M. trogodermae and 
infection rates as influenced by transmission, dosage, and host species (Schwalbe et al. 1973a and b, 
1974). The infection rates varied among the six species of Trogoderma that were studied. In 1974, 
the use of pheromones to lure insects to a pathogen inoculation device was proposed (Burkholder and 
Boush 1974). In theory, the spore-laden insects would eventually return to their natural habitats and 
infect others of the same species. The theory was successfully tested in experiments in which T. 
glabrum males were lured by the synthetic female sex pheromone to inoculation devices containing 
the protozoan spores. The males subsequently transmitted the spores to females and to the later 
generations (Shapas et al. 1977; Burkholder and Shapas 1978; Burkholder 1981). 


HONEY BEE DISEASE INVESTIGATIONS LABORATORY, LARAMIE, WY. By William T. 
Wilson 


The first USDA field laboratory in apicultural research was established in Laramie, WY, in 1926 
under the name Intermountain States Bee Culture Field Laboratory in cooperation with the 
University of Wyoming (Anonymous 1926). The first director was A.P. Sturtevant, a bacteriologist 
and bee disease specialist. The microbial control laboratory and staff offices were located on campus 
while the "honey house" (field laboratory and workshops) was situated on the university's agronomy 
farm. The primary reason for establishing the facility in Laramie (elevation of 7200 feet) was the 
total separation from commercial beekeeping. Since there were no suitable controls for the infectious 
diseases of honey bees (e.g., American and European foulbrood), except burning of the entire colony, 
it was necessary to study the diseases in an isolated area (Hitchcock 1966). The name of the 
laboratory was later changed to Honey Bee Disease Investigations Laboratory. Sturtevant retired in 
1958 (Anonymous 1959) and J.D. Hitchcock became director of the laboratory. 


Many of the early field studies on genetic stocks of honey bees with heritable resistance to American 
foulbrood disease caused by Bacillus larvae were made by Sturtevant and his associates at Laramie, 
where the resistance of honey bee larvae to the bacterium was first proven to be related to larval age 
(Woodrow 1941a; Hitchcock 1958) and the ability of adult bees to reduce the spore content of 
ingested honey through selective filtration in the honey bee stomach (Sturtevant and Revell 1953). 
The Laramie staff was involved in the development of the Island Hybrid which was the first semi- 
resistant stock of bees that became commercially available to beekeepers (Sturtevant 1949). Basic 
studies on B. Jarvae spores for tolerance to heat (Burnside 1938) and other factors were 
accomplished (Sturtevant 1930). A milk test for the diagnosis of American foulbrood based on 
proteolytic enzymes was developed at Laramie (Holst 1946). A unique study in bee pathology 
showed the behavior of worker bees towards brood infected with American foulbrood (Woodrow 
1941b). The first description of a rare gregarine parasite of honey bees was another significant 
contribution (Hitchcock 1948). Hitchcock studied the yearly occurrence of Nosema apis, 
Malpighamoeba mellificae and species of Acarapis mites (excluding Acarapis woodi) in honey bees 
shipped to Laramie from the Gulf States and in colonies wintering in Wyoming (Hitchcock, personal 
communication 1992). Most of this work was accomplished in the 1930s through the 1950s. 


Starting in the 1960s with the employment of H. Shimanuki and J.0. Moffett, basic microbiological 
and applied field studies were expanded. Staff contributions concerned the relative resistance to 
certain antibiotics of different strains of bacteria that cause bee diseases (Lehnert and Shimanuki 
1981), descriptions of hemocytes in bee hemolymph and other studies of bee blood (Gilliam and 
Shimanuki 1967, 1970, 1971), discovery of a new antibiotic (tylosin lactate) for control of American 
foulbrood (Hitchcock et al. 1970), techniques for gas sterilization of wax combs, studies towards the 
possible control of various bee viruses, factors affecting the spread and control of protozoan diseases 
(nosema and amoeba) (Moffett et al. 1969), and pathogenicity of various bacteria and fungi to the 


alkali bee (Shimanuki, unpublished data). Both Shimanuki and Moffett transferred to other ARS 
laboratories in the late 1960s. 


328 


W.T. Wilson joined the laboratory in 1968 and expanded the program on the etiology and control of 
American foulbrood. Through a courtesy appointment to the Graduate Faculty at the University of 
Wyoming, Wilson expanded the graduate student program at the ARS facility. Soon after his arrival, 
he developed a new technique for administering antibiotics to honey bee colonies that enhanced the 
efficacy of Terramycin for foulbrood control (Wilson et al. 1970, 1971; Wilson and Elliott 1971). 
This technology transferred rapidly to industry and over a period of more than 20 years antibiotic 
extender patties have saved the beekeeping industry millions of dollars through less foulbrood and 
improved colony health. Currently the patties show some value in the control of A. woodi. 


Basic bee pathology studies centered on bacterial mechanisms and pathways in American foulbrood 
(Wilson and Bitner 1970; Bitner et al. 1972) and to a lesser extent bee viruses (Nunamaker et al. 
1985). Penicillium waksmanii growth was studied as a biological control for American foulbrood 
(Tutt and Wilson 1975; Wilson et al. 1978). Hitchcock and Christensen (1972) discovered 
chalkbrood caused by Ascosphaera apis in honey bees in the central United States and the fungal 
disease was studied extensively at Laramie (Mehr et al. 1976; Menapace and Wilson 1976; 
Menapace and Hale 1984; Rose et al. 1984; Stoner and Wilson 1985). A bee disease and parasite 
survey of Mexico was accomplished in 1980 by Laramie scientists (Wilson and Nunamaker 1983; 
Wilson et al. 1984). In 1972, Wilson was appointed Research Leader. 


In February 1985, Wilson established a research program on mite control, and in May, he was 
directed by the ARS Administrator to close the Laramie Bee Laboratory and to move to Weslaco, TX 
(see above). 


EUROPEAN PARASITE LABORATORY\EUROPEAN BIOLOGICAL CONTROL 
LABORATORY, SEVRES, BEHOUST, AND MONTPELLIER, FRANCE. By Tadeusz J. 
Poprawski and Lawrence A. Lacey 


The European Parasite Laboratory (EPL) was established in France in 1919, and for many years 
USDA and cooperating scientists were stationed there to conduct exploration and other research on 
parasites and predators of arthropod pests that had become established in the U.S. (see Sections Ala 
of Chapters I-III and Bla of Chapter IV). In 1981, an insect pathology project was initiated for the 
first time at an ARS overseas laboratory, at EPL, then located at Sevres, a suburb of Paris, France. 
The purpose of the project was to find and evaluate species and strains of exotic entomopathogens 
present in Europe that would have potential for use against insect pests in the United States. The 
research was conducted under cooperative agreements between ARS and other agencies, since there 
was no permanent position for an insect pathologist. 


G.C. Soares, Jr., was the first scientist in charge of the pathology program. He was stationed at the 
Biological Control Research Laboratory of the French National Institute for Agronomic Research 
(INRA) at La Miniére, near Versailles, from October 1, 1981, to November 30, 1982, working under 
a Cooperative Agreement between ARS-EPL and INRA. During his tour, Soares worked on EPL 
program pests, including Otiorhynchus and Sitona weevils (Soares et al. 1983; Aeschlimann et al. 
1985), and sent a number of shipments of insect viruses and fungal pathogens to ARS locations at 
Beltsville, MD, and Ithaca, NY, respectively, for further evaluation. Soares prepared a 67-page report 
of the project, which is unpublished but on file at the ARS Biological Control Documentation Center 
(BCDC), Beltsville, MD, and the European Biological Control Laboratory (EBCL), Montpellier, 
France. 


In 1983, T.J. Poprawski began conducting pathology research in Europe under a USDA-INRA 
Cooperative Agreement, which terminated March 30, 1984. He continued to study entomopathogens 
of EPL's program pests, including Otiorhynchus and Sitona weevils, gypsy moth, onion maggot, 
Heliothis/ Helicoverpa species, and filth flies (Poprawski et al. 1985a, b, and c), and sent numerous 


ono 


shipments of fungal pathogens to the ARS location at Ithaca. He also prepared a second report of the 
project; this 74-page unpublished report is also available at Beltsville and Montpellier. In April 1984, 
Poprawski left to spend a one-year training session on the Entomophthorales at the ARS Insect 
Pathology Research Unit at Ithaca, NY, under the direction of Richard S. Soper. 


I. Majchrowicz, on leave from the Polish Academy of Agriculture's Department of Entomology at 
Szczecin, Poland, filled the vacant pathology position from April 1 to September 30, 1984, under 
another joint research agreement (with INRA), and prepared the third, 60-page, report of the project. 
R. Le Brun, on a sabbatical from the University of Rhode Island, worked at EPL from September 1, 
1984, until August 23, 1985. His main duty was to help establish the Insect Pathology Unit 
Laboratory at EPL's new location in Béhoust, a small village about 40 km west of Paris. N.K. 
Maniania was employed as a pathology technician from February to October 1984 under the 
ARS-INRA agreement. When this agreement was terminated in October 1984, Majchrowicz returned 
to Poland and Maniania joined EPL's staff as temporary pathology technician. 


After training in the U.S., Poprawski returned on April 1, 1985, to the EPL at Béhoust, under a 
Specific Cooperative Agreement with Boyce Thompson Institute for Plant Research, Ithaca, until 
August 1, 1987, and as an ARS Research Entomologist thereafter. His first duty was to finalize 
establishment of the Insect Pathology Unit laboratory, which became functional by mid-May 1986. 
Poprawski resumed explorations for and research on pathogens of a number of insect pests, including 
the onion maggot, filth flies, Empoasca vitis, Sitona and Otiorhynchus weevils, southern green stink 
bug, and range grasshoppers. Research included, but was not limited to, bioassays of fungal 
pathogens and their toxic metabolites, interactions of parasites and fungal pathogens in arthropod 
control, safety of fungal pathogens to beneficial insects, genetic variability of fungal isolates, and 
impact of chemical pesticides on fungal pathogens (Riba et al. 1986; Poprawski et al. 1988; Goettel 
et al. 1990; Majchrowicz et al. 1990). 


From mid-April 1988 until September 22, 1990 (when Poprawski was transferred to the ARS Plant 
Protection Research Unit at Ithaca, NY), EPL pathology research was redirected primarily to the 
Russian wheat aphid and other cereal aphids. Poprawski (with F. Gruber and other EPL 
entomologists) conducted exploration for and collection of natural enemies of the aphids in Turkey, 
Bulgaria, Yugoslavia, Greece, and the Moldavian, Kirghiz, Uzbek, Kazakh, and Ukrainian republics 
of the former Union of Soviet Socialists Republic. Explorations in the former U.S.S.R. were 
conducted under the auspices of a newly established joint U.S.A—U.S.S.R. program on biological 
control of pests. Numerous shipments of aphid fungal pathogens were sent to the ARS laboratory at 
Ithaca. (Parasites and predators were also shipped to several ARS, APHIS, and university locations in 
the U.S.) Reports of the explorations were prepared and are on file at Beltsville and Montpellier. 
Additionally, research projects concentrated on the interaction of parasites and fungal pathogens of 
Russian wheat aphid. Poprawski determined, through bioassays, the relative pathogenicity of 
naturally occurring aphid pathogens to Russian wheat aphid and its parasites. Studies were also 
conducted to determine the influence of the introduction of various parasite and pathogen 
combinations on Russian wheat aphid populations. Entomophthoralean fungi, primarily Zoophthora 
radicans and Pandora neoaphidis, along with other species collected, were utilized in these studies, 
and bioassayed against Aphelinus and Aphidius parasite species. These studies were useful to 
evaluate potential introductions of pathogens and parasites into the U.S., as well as forming a basis 
for future research both at EPL/EBCL and in U.S. laboratories (Kiriac et al. 1990; Gruber et al. 1991; 
Kovalev et al. 1991; Poprawski et al. 1992a, b, and c). 


The insect pathology program became an integral, ARS-funded part of the ARS overseas program at 


the time of the consolidation of the two ARS European laboratories (Béhoust and Rome) at 
Montpellier, France, in September 1991 (see Chapter IV), and with the assignment in October 1991 


330 


of L.A. Lacey to the newly established EBCL; Poprawski served as advisor for the program from his 
departure until Lacey's arrival. 


Establishing and outfitting the pathology laboratory and foreign exploration for natural enemies of 
the sweetpotato whitefly (SPWF) and Russian wheat aphid (RWA) and other cereal aphids has been 
the principal activity of EBCL's Pathology unit since Lacey's arrival. Collections of pathogens and 
other natural enemies have been made over a broad geographic range (Spain, Greece, France, Russia, 
Egypt, Pakistan, India and Nepal) and under diverse climatic and environmental conditions. Several 
isolates of Paecilomyces fumosoroseus and other fungi from SPWF from the Indian subcontinent and 
several Hyphomycetes and Entomophthorales have been isolated from RWA and other cereal aphids 
in France, Spain, Russia, and the Indian subcontinent. Isolations of pathogens also were made from 
orchard and urban pests including codling moth, gypsy moth, and thrips. 


In addition to collecting and shipping activities, research was started on the effects of a variety of 
environmental parameters that enhance or limit the activity of fungal pathogens of Homoptera. 
Numerous fungal isolates have been sent to the ARS Collection of Entomopathogenic Fungal 
Cultures (ARSEF) at Ithaca, NY. 


Cooperative relations in most of the host countries where collections have been made during 1991- 
1992 have resulted in additional collection and shipment of natural enemies to EBCL and the U.S. It 
is envisioned that cooperative efforts will continue in southern India, Pakistan, Crete, and Spain, 
along the lines of applied studies and student exchange. 


In the Montpellier area cooperative relations have been established with scientists of INRA, Centre 
International de Recherche Appliqué et de Développement (CIRAD), and Ecole Nationale Supérieure 
Agronomique de Montpellier. The EBCL Pathology Unit is developing a cooperative program with 
Jacques Fargues and other INRA colleagues recently assigned to Montpellier from the INRA 
Laboratory in La Miniére. 


JAPANESE BEETLE CONTROL PROGRAM, AZORES, PORTUGAL. By Lawrence A. Lacey 


The Japanese beetle control program on the island of Terceira (Azores, Portugal) was implemented 
under the direction of USDA-ARS International Activities (now Office of International Research 
Programs). Michael G. Klein (USDA-ARS, Wooster, Ohio) has been advising the Azorean 
Department of Agriculture and the University of the Azores on the use of biological control agents 
for control of the beetle since 1984. From January 1990 until October 1991, Lawrence A. Lacey was 
assigned to the island to implement a biological control program based on insect pathogens and 
parasitic insects (Lacey et al. 1994; Mendes et al., 1994). Transfer of proven technology was a key 
goal of the project. Research in a number of areas still is required in order to determine the best 
suited natural enemies for effective control. To this end, efficacy and other studies have been 
conducted on a number of pathogens (bacteria, fungi, protozoa) and parasites (nematodes, 
arthropods) (Lacey et al. 1993). The most efficacious control agents against larvae are the nematode, 
Steinernema glaseri and the fungus, Metarhizium anisopliae. The construction of a laboratory and 
pathogen production facility was completed prior to Lacey's departure. The facility enhances 
continuation and expansion of the project's control activities on a sustained basis. Lacey and Klein 
continue to be involved in the Azores project through field work and advisory activities. Increased 
exploration for pathogens and parasites of the beetle in Japan and China and their utilization in the 
island's control program will be the main ARS activity over the next few years. 


5181 


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394 


APPENDIX III 
DETAILED HISTORY OF BIOLOGICAL CONTROL 
IN THE FOREST SERVICE 
Edited by M. E. Dix 


I. PREFACE. By Mary Ellen Dix 


The Overview (Chapter V) and Appendix III summarize Forest Service research and control efforts 
with biological agents from 1953 to 1993; some earlier studies are also discussed. The overview 
briefly describes trends and directions of biological control activities. Appendix III is an in-depth 
review of research and control efforts on specific insects and groups. However, the appendix is not 
all inclusive. It includes efforts on major pests, long-term studies on natural control agents, studies 
that had unique outcomes, and applications of biological control agents. Small studies that identified 
natural enemies of minor pests and determined their impact, or those that involved implementation of 
a biological control technique were not included unless they were part of a larger effort on a forest 
pest. Some taxonomic revisionary studies (e.g., Schmid 1969b; Torgersen 1974), and other notes on 
the identity and biology of natural enemies (e.g., Wickman 1964; Harman and Kulman 1967; Schmid 
1970b; McKnight and Tagestad 1972; Mitchell and Maksymov 1977; Pasek and Kearby 1984; 
Galford 1985; and Thompson and Solomon 1986) also were excluded from this appendix. 


Appendix III is generally arranged by damage category and pest. Exceptions are the sections on mites 
and nematodes, and on Bacillus thuringiensis, where long-term progress crosses pest species 
boundaries. As in other parts of this book, complete scientific names of all organisms mentioned in 
the text are given in the Taxonomic Index for the entire publication. 


II. BIOLOGICAL CONTROL OF ARTHROPODS 
A. Bark Beetles (Coleoptera: Scolytidae) 
1. Black turpentine beetle, Dendroctonus terebrans (Olivier). By Mary Ellen Dix 


The black turpentine beetle (BTB) is a native pest of slash pine and longleaf pine in the southern 
U.S. Many Forest Service (FS) scientists evaluated native endoparasitic nematodes, clerid beetle 
predators, and extraregional mites (Moser and Dell 1980; Moser 1981; Kinn 1984a and b; Moser and 
Bogenschutz 1984; Moser et al. 1978) for suppression of BTB. Although these natural enemies may 
have considerable impact on BTB populations, they often are ineffective during epidemics. Miller et 
al. (1987) identified an exotic coleopteran predator, Rhizophagus grandis, as a potential control 
agent. This beetle is a predator of the European spruce beetle in England, Europe, eastern Siberia, 
and Turkey (Bevan and King 1983). In 1985, Gregoire et al. (1986) demonstrated that R. grandis was 
attracted to frass produced by its European host and to frass produced by three species of native 
North American bark beetles, BTB, southern pine beetle (SPB), and spruce beetle. Moser selected R. 
grandis for importation and release against the BTB because both BTB and D. micans have long life 
cycles and gregarious larvae. If successful, R. grandis could also prey on SPB (Moser 1989). 


Sey 


In 1986 and 1987, Gregoire shipped 300 pairs of R. grandis from Belgium to the USDA Forest 
Service Forestry Center at Pineville, near Alexandria, LA, to test methods for rearing the predator on 
BTB and SPB and obtaining sterilized eggs. The semi-artificial rearing method selected involved 
raising R. grandis in plexiglass sandwiches inoculated with about 20 BTB larvae (Moser 1989). The 
resulting predator eggs were surface sterilized in White's solution (Barras 1972) to reduce the chance 
of introduction of microorganisms from Europe. During 1987, this method was used to mass produce 
R. grandis in the laboratory and the first 20 pairs of the beetle were released in April 1988 (Moser 
1989). The establishment and potential long-term impact of R. grandis on the BTB populations is not 
known. 


2. Douglas-fir beetle, Dendroctonus pseudotsugae Hopkins. By Mary Ellen Dix 


During the 1950s, the Douglas-fir beetle seriously threatened stands of Douglas-fir, the leading 
commercial tree species in the U.S. In 1956, Forest Service's Intermountain Forest and Range 
Experiment Station initiated a long-term study on the ecology and biology of the beetle and on its 
natural enemies (Furniss 1967). Massey (1956) identified nematode parasites of the beetle (see also 
section on Mites and Nematodes). Between 1958 and 1962, Furniss examined nematode parasitism 
rates and found that they varied little by sex but varied with localities, standing and felled trees, and 
maturity of beetles (Furniss 1967). During this same period, Ryan evaluated the biology, habits, and 
embryology of the braconid parasite Coeloides brunneri in western Oregon and identified possible 
means to manipulate C. brunneri populations for controlling the Douglas-fir beetle (Ryan and 
Rudinsky 1962; Ryan 1963). In 1959, adult beetles were found to be parasitized by the pteromalid 
Karpinskiella paratomicobia. However, Furniss (1968) found that parasitism may actually increase 
the survival rate of the beetle's offspring. Oregon State University published a technical bulletin that 
described and identified the immature stages of Douglas-fir beetle parasites and predators (Kline and 
Rudinsky 1964), part of the results of a cooperative university-Forest Service study. 


3. Spruce beetle, Dendroctonus rufipennis (Kirby). By Mary Ellen Dix 


Since 1898, periodic epidemics of the spruce beetle (Dendroctonus rufipennis, formerly known as the 
Engelmann spruce beetle, D. enge/manni) occurred in the Rocky Mountains and the Pacific 
Northwest. Initial studies on biological control of the spruce beetle targeted identification of natural 
enemies and assessment of their impacts. 


In 1941, the Division of Forest Insect Investigations of the Bureau of Entomology and Plant 
Quarantine (BEPQ) and the Colorado Agricultural and Mechanical College initiated a study to obtain 
data on the beetle's life history and habits and to develop practical control methods for massive 
outbreaks. Massey and Wygant (1954) summarized the results of this study and identified important 
natural enemies and their impacts. They reported that woodpeckers could locate and destroy up to 
75% of the brood, while hymenopteran, dipteran, and coleopteran natural enemies could locate and 
destroy up to 50% of the brood. 


A 1947 BEPQ study identified prey of woodpeckers and sapsuckers by analyzing the stomach 
contents of 135 birds in Colorado. Sixty-five percent of the arthropods in the birds' stomachs were 


spruce beetles, 13% were other scolytids, 12% were formicids, and 6% were cerambycids (Massey 
and Wygant 1954, 1973). 


After another severe outbreak of spruce beetle in Colorado during the 1960s, the Rocky Mountain 
Forest and Range Experiment Station funded several studies with Colorado State University to learn 
more about the natural enemies of the spruce beetle. Seven species of parasites were successfully 
reared and a taxonomic key to larvae was developed (Jensen 1967). During observations of 
woodpecker behavior in infested stands, it was found that abundance of three-toed, hairy, and downy 


396 


woodpeckers was closely related to beetle abundance. Pairs of woodpeckers often confined their 
activities to small areas of infested stands (Baldwin 1968a and b; Koplin and Baldwin 1970). 
Subsequent studies assessed the effects of stand densities on woodpecker predation (Shook and 
Baldwin 1970; Koplin 1972). 


The current outbreak of spruce beetles in Alaska and northwestern Canada began in the mid-1980s. 
Although parasites have been identified, research has concentrated on the use of silvicultural and 
other management techniques. 


4. Mountain pine beetle, Dendroctonus ponderosae Hopkins. By Richard F. Schmitz 


Except for one attempt to introduce an exotic predator, biological control efforts directed against the 
mountain pine beetle (MPB) on lodgepole pine concentrated on identifying and assessing the relative 
abundance and effectiveness of native predators and parasites. Recent studies evaluated predator 
responses to pheromones and kairomones produced during beetle colonization of the host tree. 


Current understanding of the biology, abundance, and impact of entomophages on MPB in lodgepole 
pine was gleaned from earlier studies by BEPQ entomologists at the Forest Insect Laboratory at 
Coeur d'Alene, ID, on MPB bionomics and ecology, and on the enhancement of native natural enemy 
species. These studies, combined with results of later studies in lodgepole pine, western white pine, 
and ponderosa pine, provided the understanding needed to ensure that potential introductions of 
exotic beneficial species did not adversely impact native beneficial species. Basic biologies of the 
biological control agents found in the three host trees are similar. A key to the common parasites and 
predators of the MPB in these host species was prepared by Rasmussen (1976). 


Insect parasites and predators. Bedard (1939, 1940, 1942) and DeLeon (1929, 1930, 1931, 1934a and 
b, 1935a and b) conducted most of the early studies on the biology, distribution in the host tree, and 
relative effectiveness of insect parasites and predators in western white pine and lodgepole pine. 
DeLeon (1931) described the developmental stages, aspects of the biology, and effectiveness of 
parasites, predators, and other associated insects of the beetle on western white pine. In 1934, he 
published an annotated list of the parasites, predators, and other fauna associated with the beetle in 
western white and lodgepole pines (DeLeon 1934b) (Table 1). Almost 50 years later Chatelain and 
Schenk (1983) conducted a similar study to determine relative abundance and within-tree distribution 
of insects inhabiting MPB-infested lodgepole pine in central Idaho and northeastern Oregon. Results 
of this study were similar to those described by DeLeon (1934b) and Amman and Cole (1983). 
DeLeon and subsequent investigators considered the following Hymenoptera to be most important 
parasites of MPB: Coeloides dendroctoni, Dinotiscus (as Cecidostiba) dendroctoni, D. acutus, D. sp., 
and Roptrocerus xylophagorum (as Pachycerus eccoptogastri). 


Parasitism of MPB by C. dendroctoni averaged about 16% (DeLeon 1931). DeLeon (1931, 1935a) 
considered this braconid to be the most important parasite of MPB brood because most larvae were 
parasitized when they were about to pupate and had a high probability of reaching the adult stage. 
Investigations of the life stages, biology, and effectiveness of Coeloides spp. were more complete 
than similar studies on the remaining parasites (DeLeon 1934a, 1935a). 


DeLeon (1931) ranked the dipterous predators as the second most important natural control, followed 
by certain coleopterous species. The dolichopodid, Medetera aldrichii, fed on almost any species of 
larva, including its own, and was considered the most important dipteran predator (DeLeon 1935a). 
However, cannibalism by M. aldrichii larvae adversely affected predator abundance. Medetera 
aldrichii \arvae either partially consumed MPB larvae before abandoning them to search for more 
prey, or consumed most of the larvae. Predators that only partially consume a prey have been shown 
to destroy more prey than those that entirely consume each prey (Amman and Cole 1983). Nagel and 


397 


Fitzgerald (1975) found that when prey are scarce, M. aldrichii larvae consume most of each prey 
before seeking another, suggesting this behavior may be density-dependent. Overall, M. aldrichii was 
considered to be less effective than C. dendroctoni because many of the immature beetle larvae 
destroyed by M. aldrichii in the fall would probably have died from other causes before maturing. 


Despite the abundance of predaceous adult and larval clerid beetles (DeLeon 1934b; Reid 1957), 
DeLeon (1934b) discounted their impact on MPB brood survival. More recent laboratory studies 
have established their potential effect on MPB survival. Schmid (1970a) found that each Enoclerus 
sphegeus adult killed one MPB adult per day, and Amman (1970) found E. sphegeus larvae 
consumed an average of 16 large or 38 small MPB larvae while completing development. Larvae of 
another clerid, Tanasimus undatulus, consumed an average of 18 large or 35 small MPB larvae to 
complete development (Amman 1972). The effectiveness of adult clerids in preying upon adult MPB 
as they colonized trees has not been measured. 


In laboratory rearings, parasites and predators destroyed between 2.5 and 6.5% of the MPB eggs 
contained in log sections cut from field-infested trees during four summers (Amman and Cole 1983). 
Nematodes, parasites of both mature and immature MPB, destroyed the most eggs (1.13 to 4.06%) 
(Massey 1966a, b and c). This loss was fairly evenly distributed thoughout the galleries. The 
nematode Mikoletzkya pinicola was identified by Massey as the only nematode present in cultures 
established from these laboratory rearings and was observed preying on MPB eggs (Amman and Cole 
1983). Unidentified fungi caused the second greatest loss of eggs (0.76 to 1.80%), with the greatest 
loss usually occurring in the first few inches of the gallery (Hunt et al. 1984). Unidentified mites 
accounted for predation of only two eggs (0.06%) during one season. Most mites appear to be 
saprophytic (fungus feeders), or, if predaceous, fed on other organisms under the bark (Rust 1933, 
1935). Predatory mites were not found during examination of MPB populations in Colorado and 
South Dakota (Boss and Thatcher 1970). 


Although not included in these studies, M. aldrichii may destroy 40 to 50% of MPB eggs (DeLeon 
1935a). Schmid (1971) reported M. aldrichii |arvae preyed on eggs in the first few inches of the egg 
gallery and consumed from 12 to 25 eggs each during 15 days of laboratory rearing. 


Abundance of MPB in relation to bole infestation patterns. During the 1930s, Bedard evaluated 
factors regulating the abundance of MPB within the tree. He found that the abundance of beetle 
brood and associated insects along the bole of infested western white pine trees varied with tree 
species and among trees. Distribution of MPBs among trees seemed related to bark thickness with 
thicker-barked trees having more brood, and infested length within a tree varied with bark thickness, 
tree diameter and height. MPBs were most abundant in the thicker bark located in the basal portion 
of the tree (Bedard 1937). 


Distribution of predators was similar to that of MPB; predators were more numerous where beetle 
brood densities were the highest. The parasite C. dendroctoni also was most abundant where larval 
densities of MPB larvae were the highest and the bark was thin enough for oviposition. Parasites that 


use ventilation or entry holes for oviposition were most abundant in the thicker-barked portion of the 
tree. 


MPB survival was measured in endemic, epidemic, and postepidemic infestations (Amman 1984). 
Significantly more MPB (P <0.01) survived in endemic (3.7%) infestations than in epidemic (1.4%) 
and postepidemic (0.5%) infestations. Natural enemies accounted for 8, 33, and 4% of total MPB 
losses in endemic, epidemic, and postepidemic infestations, respectively. The greatest predation of 
MPB at epidemic levels was attributed to larvae of the dolichopodid fly M. aldrichii (13%) and 
woodpeckers (15%). Interestingly, although mortality caused by most predators and parasites was 


398 


density-dependent, clerid predation was not. Clerids consumed a greater percentage of MPB larvae at 
endemic infestation levels, but accounted for only 0.9% of the brood mortality. 


Cole (1981) and Amman and Cole (1983) compared measures of component probabilities for MPB 
brood mortality in infested lodgepole pine forests in the Intermountain Region that were ascribed to 
11 specific mortality factors including five natural enemies. Probabilities of death were computed for 
each factor during pre-epidemic, epidemic, and post-epidemic stages. These data revealed that lethal 
winter temperatures and drying of the phloem in the early summer, and not natural enemies, were the 
two major causes of MPB brood mortality. Medetera aldrichii apparently was the most important 
natural enemy because predation increased with MPB brood density during pre-epidemic and 
epidemic stages of infestation, and with increasing MPB brood densities associated with increasing 
tree diameters. These findings suggest that predation by M. aldrichii larvae is a significant factor in 
reducing MPB brood survival in large-diameter trees during the post-epidemic period. In contrast, 
larval predation by the clerids Thanasimus undatulus and Enoclerus sphegeus was negligible. Impact 
of predation by adult clerids on adult MPB while initiating attacks on a tree was not measured. 
Probability of parasitism by C. dendroctoni increased with brood density in 9-inch (23-cm) diameter 
trees, and decreased with brood density in 12-inch (30-cm) diameter trees (Cole 1981; Amman and 
Cole 1983). 


Overall predation by woodpeckers was low. The greatest woodpecker predation occurred during the 
pre-epidemic stage in the 12-inch (30-cm) or smaller diameter trees when the entire woodpecker 
population searched the few infested trees. However, as the beetle population became epidemic, the 
woodpecker population did not increase proportionally to the beetle population and consumed 
proportionally less of the beetle population. In the post-epidemic stage, woodpeckers did not 
consume proportionally as many beetles as they did during the pre-epidemic stage. Low woodpecker 
predation levels in 15-inch (38-cm) trees was probably due to increased difficulty in removing larvae 
from the thicker bark (Cole 1981, Cole and Amman 1985). 


Bedard (1938) found that MPB brood mortality from natural enemies was constant on all four sides 
of the tree, although MPBs were most abundant on the north and east sides of western white pine in 
1935 and on north and west sides in 1936. 


Natural enemy effectiveness. Bedard (1939) evaluated the overall impact of natural enemies on MPB 
populations. He found that parasites destroyed an average of 54% of the brood in windfelled trees, 
and 65% of the brood in standing trees. MPB populations were reduced when 21 or more individual 
natural enemies were present per ft” (930 cm’) of bark surface. He recommended against chemical 
treatment of windfalls when 30% of the brood were parasitized or when there were parasites in the 
base of standing trees (Bedard 1933b). 


Effectiveness of Coeloides dendroctoni was limited by parasite behavior, life cycle, and reproductive 
potential, hyperparasitism, and bark thickness (DeLeon 1935b). The parasites usually were found in 
Ips-infested pines and were not present in sufficient numbers during the first few years of a MPB 
infestation to destroy many of the larvae. Their abundance increased slowly. Most C. dendroctoni 
remained in the tree almost a year after the host beetles were killed and then stayed within the 
original "epicenter" of infestation instead of moving into the outlying groups of MPB infested trees. 
Many C. dendroctoni were hyperparasitized by Eurytoma sp. and Gelis sp. 


Accessibility of the beetle brood influenced abundance of beneficial species. Bedard (1939) found 
that beneficial insects were not equally distributed among trees comprising an infestation. Parasites, 
which oviposit through the bark, were most abundant in thin-barked trees, while predators were most 
abundant in thick-barked trees (Bedard 1939; Dahlsten and Stephen 1974). Thick-barked sugar pine 
had few parasitized beetles and large numbers of predaceous beetle larvae (Struble 1942). 


399 


The effect of predators on flying beetles is difficult to measure. The robber fly Laphria gilva killed 
about 1% of flying MPB in ponderosa pine stands of the Black Hills (Schmid 1969a) and were 
captured in large numbers in passive traps in MPB-infested lodgepole pine stands (R.F. Schmitz; data 
on file at Forestry Sciences Laboratory, Ogden, UT, January 1981). 


Parasites were found to be most abundant in trees where the MPB brood was in stages suitable for 
oviposition (Bedard 1939). Parasites were most abundant in western white pine in August because 
the larvae were suitable hosts at that time when most parasites were ready to oviposit. In contrast, 
MPB adults in lodgepole pine do not mature until late May or June and their larvae were too 
immature to be parasitized in August. In addition, western white pine growing on moist sites were 
shown to have more natural enemies than those growing on dry sites, leading Bedard (1939) to 
recommend that these "reservoir" white pine trees growing on moist sites be left untreated during 
chemical control programs. 


Augmentation using semiochemicals. The responses of beneficial insects to synthetic 
semiochemicals used to manipulate MPB populations were measured by Borden (1974, 1977) and 
Lindgren and Borden (1989). Chatelain and Schenk (1983) evaluated the use of synthetic attractants 
to augment abundance of these beneficials in lodgepole pine stands in central Idaho and northeastern 
Oregon. The clerid predator Thanasimus undatulus responded to sticky traps baited with either 
frontalin or exo-brevicomin (Chatelain and Schenk 1984). Abundance of 7. undatulus adults was 
increased on pines baited with frontalin before (May to mid-July) or during (mid-July to September) 
the MPB flight period. Baiting the trees before the bark beetle flight period was the most effective 
augmentation method because baiting was concurrent with peak 7: undatulus flight activity but 
before the onset of peak MPB flight. This technique assured that this predator was attracted to the 
study trees before competing sources of attraction were created by MPB infestation of nearby non- 
study trees. Baiting brood trees in this manner increased the incidence of T. undatulus larvae 
threefold and mortality of emerging MPB adults by 7.1%, but did not significantly reduce MPB 
brood survival or consequent tree mortality. Thus, frontalin could be used to increase substantially 
the predator population and to enhance other control tactics within a pest management program 
(Chatelain and Schenk 1984). Such attempts would likely be more feasible at low or endemic levels 
of MPB. 


Avian predators. The impact of birds on MPB populations during the flight period can be substantial 
(Rust 1929, 1930). The stomachs of 15 of 18 birds caught in lodgepole pine forests contained from 
one to 289 MPB. MPB represented up to 20% of the food volume. In 1929, nighthawks consumed the 
most MPB, an average of 76 MPB/bird (n=10), but their impact was minimal because of their limited 
occurrence. Three-toed and hairy woodpeckers averaged only two MPB/bird (n=5), but had a greater 
impact because they were more abundant. However, in 1930, quantities of beetles taken by 
nighthawks and woodpeckers were reversed because the MPB infestation moved to another area. 
Nighthawks averaged only five beetles (n=14), because they stayed within their established breeding 
grounds. Woodpeckers averaged 33 beetles/bird (n=8), because they moved with the MPB outbreak. 


Birds can have a substantial impact on flying MPB populations. Stallcup (1963) censused birds and 
analized their stomach contents in a ponderosa pine stand in Colorado. He estimated that birds 
consumed 8.5% of adult MPB during their flight period and identified additional species of bird 
predators (Table 1). Woodpeckers consumed numerous MPB and caused the desiccation of many 
more by exposing the larvae when opening the bark. Prey size is an important factor affecting 
predation by woodpeckers, which avoid trees containing small larvae and concentrate on trees 
containing large larvae (Koplin and Baldwin 1970). At high elevations in northwest Wyoming, 
woodpeckers preyed mostly on parent beetles because of the small size of larvae (Amman 1973). 
During epidemics, woodpeckers are believed to have an insignificant effect on MPB populations 


400 


(Berryman 1976). However, during endemic periods, they may play an important role in keeping 
populations in check. 


Nematode parasites. Massey (1957), Steiner (1932), and Thorne (1935) described nematode parasites 
of MPB and made observations on their biologies and habits (see also Mites and Nematodes section). 
Reid (1958) studied the influence of the nematode Sphaerulariopsis hastata and found a one-third 
reduction in number of eggs produced by infested beetles. 


Introduction of an exotic predator. In July 1982, an attempt was made to introduce an exotic predator 
as a biological control agent against MPB in lodgepole pine in the Intermountain Region. R.F. 
Schmitz, a research entomologist assigned to the MPB research work unit located at Ogden, UT, 
obtained a dipterous predator of larvae, Palloptera modesta (as parallela), from the ARS Beneficial 
Insects Research Laboratory in Newark, DE, originally received from the USSR. He released the 
predator in an active MPB infestation that was building to outbreak levels on the north slope of the 
Uinta Mountains in the Burnt Fork Drainage of the Wasatch National Forest, UT. The adults were 
received just prior to the onset of peak MPB flight and attack and were released in mid-July on caged 
lodgepole pine that had been attacked in May by the pine engraver and a few MPB. One 6-inch by 
12-inch (15.2-cm by 30.4-cm) bark sample was removed from the caged area on each tree after 
release of the predators. Examination of these samples revealed abundant bark beetle brood but no 
predaceous Palloptera larvae. Final evaluation was scheduled for the spring of 1983. Unfortunately, 
record-breaking warm temperatures and heavy rains combined to produce extremely heavy spring 
runoff that destroyed bridges and roads, preventing access to the release area. This prevented bark 
samples from being removed prior to anticipated predator emergence from the trees included in the 
release. There have been no further attempts to establish this predator. (R.F. Schmitz, unpublished 
data; Coulson 1992.) 


Conclusions. Most measurements of the incidence, distribution, and relative effectiveness of 
beneficial agents were made at epidemic levels of MPB, when beetle populations were the least 
manageable. The population dynamics of these beneficial agents need to be evaluated at low or 
endemic levels of MPB. Also, efforts to assess the effects of synthetic bark beetle semiochemicals on 
the ecology and diversity of beneficial species need to be expanded, especially for semiochemicals 
used to suppress beetle populations. Because many beneficial insect species can prey upon or 
parasitize several bark beetle species, use of attractants to concentrate bark beetle populations for 
suppression purposes is likely to disrupt the natural distribution of the associated beneficial species. 
There is a need to develop methods for measuring the impact of such treatments on the distribution 
and effectiveness of beneficial agents. 


5. Smaller European elm bark beetle, Scolytus multistriatus (Marsham). By Mary Ellen Dix 


The smaller European elm bark beetle (SEEBB) is the primary vector of Dutch elm disease in 
American elm. The beetle was first discovered in the U.S. near Boston, MA, in 1909 and since then 
has spread from coast to coast (Chapman 1910). Both importation and release of foreign parasites 
and augmentation of native parasites have been studied as control measures. 


During 1964 and 1965, three species of braconid parasites were sent from France to the Forest 
Service's Central States Experiment Station Laboratory in Delaware, OH (USDA Forest Service 
1965). In the fall of 1964, a laboratory culture of the braconid Dendrosoter protuberans was 
established there on SEEBB. In the following months, the parasite was successfully mass-produced 
on these beetles. During the summer of 1965, B.H. Kennedy released and successfully recovered D. 
protuberans (USDA Forest Service 1966; Kennedy 1970). Subsequent studies determined that D. 
protuberans overwintered and competed favorably with three native parasite species (Kennedy 
1970). Interspecific competition among the parasites for hosts was later found to impact adversely 


401 


parasite abundance. If larvae of the native parasite Entedon leucogramma have matured enough on a 
host before D. protuberans oviposited on the same host, the immature E. /eucogramma larvae will 
survive (Kennedy 1981). 


By 1967, a technique was developed for rearing E. Jeucogramma and also D. protuberans from 
SEEBB raised on artificial media (Galford 1967; Kennedy and Galford 1972). This technique could 
be used to mass-rear other SEEBB parasites. In addition, it was found that the SEEBB parasites £. 
leucogramma, Spathius benefactor, and Cheiropachus colon were attracted to Multilure™, a 
commercial pheromone used to attract and trap SEEBB. Because large numbers of parasites could be 
caught on sticky traps baited with this attractant, Kennedy recommended delaying SEEBB trapping 
programs until just before overwintering beetles emerged. This strategy would protect parasites that 
emerge before the SEEBB adults in the spring. The pheromone also could be used to attract parasites 
to infested trees (Kennedy 1979). 


6. Southern pine beetle, Dendroctonus frontalis Zimmermann. By Mary Ellen Dix 


The southern pine beetle (SPB) is the most destructive native bark beetle in the southern U.S. SPB 
larvae, tree pathogens carried by the beetles, or a combination of larvae and pathogens girdle infested 
trees. Tree mortality can be spectacular. Trees die within a few months of infestation, and entire 
stands can be decimated within a season (Thatcher 1981). Removal of all infested trees, and 
harvesting of uninfested trees before they reach maturity are recommended control procedures. 
Natural enemies are another possible control method. Biological control research and application 
efforts can be divided into three eras: a pre-Expanded Southern Pine Beetle Research and 
Applications Program (ESPBRAP) era, an ESPBRAP era, and a post-ESPBRAP era. 


Pre-Expanded SPB Pine Beetle Research and Applications Program. Before 1974 (pre-ESPBRAP), 
natural enemies studies by Forest Service scientists and their university and State Forest Service 
cooperators were focused on identifying SPB parasites, predators, and associates (Thatcher 1960; 
Dixon and Osgood 1961; Thatcher and Pickard 1964; Overgaard 1968; Moore 1970a and b, 1971, 
1972; Moser and Roton 1971; Moser et al. 1971a and b). Moore (1970a and b, 1973a and b) also 
evaluated pathogenicity of bacterial and fungal isolates from SPB in North Carolina. Dix compared 
relative abundance, attack height, daily activity patterns, and other aspects of the behavior and 
biology for certain hymenopterous parasites of SPB and the predator Thanasimus dubius during a 
severe outbreak in the early 1970s (Dix and Franklin 1974, 1977, 1978, 1981, 1983). Research on 
related Jps species and other Dendroctonus species was limited to identifying natural enemies and 
aspects of their biologies (Bedard 1965; Furniss 1968; Jouvenaz and Wilkinson 1970). Information 
available in 1974 on the identity and biologies of bark beetle natural enemies lacked the depth 
needed to develop realistic population models for detecting and predicting forest population trends 
and control strategies for SPB and associated Jps bark beetles. Additional expanded studies were 
needed on the impacts, biologies, and interactions of bark beetle natural enemies. 


Expanded SPB Research and Applications Program. Responding to public concern over damage 
caused by a severe SPB outbreak in the early 1970s and the lack of a comprehensive management 
strategy to address it, Congress established the 6-year ESPBRAP in 1974. Congress subsequently 
appropriated over $2 million per year to the Forest Service and USDA's Cooperative State Research 
Service (CSRS) (Shea 1985). The ESPBRAP's mission was to develop coordinated, short-term 
programs to implement available technology for reducing losses and to develop new short- and long- 
term forest pest management systems that would effectively suppress or prevent infestations. This 
program focused on understanding the population dynamics of the SPB; obtaining information 
needed to develop integrated models for predicting impacts, population levels, and forest 
susceptibility; and developing suppression techniques with pheromones and insecticides. One broad 
ESPBRAP goal was to complete studies on natural enemies that could be used as potential control 


402 


agents. This goal was later narrowed to developing sampling techniques and obtaining information 
on specific biological agents critical to understanding SPB population dynamics or predicting 
population trends (Thatcher 1981). 


ESPBRAP also funded related studies by scientists in the U.S. Forest Service, in universities, and in 
state forest services to accomplish these goals. The results were summarized by Berisford (1981) and 
were shared among investigators and other experts at formal and informal meetings. The funded 
studies can be broadly divided into the following categories: identification and sampling, population 
dynamics, and host preference. 


Initial efforts identified additional natural enemies and developed tools for their identification, and 
assessment of their impact and distribution. Moser (1975) identified 32 species of mites that were 
predaceous on SPB. Larval and adult keys for rapid identification of natural enemies were developed 
(Kinn 1976; Finger and Goyer 1978; Goyer et al. 1980). Stephen and Taha (1976) developed a 
protocol for sampling natural enemies. Other investigators determined seasonal, geographic, and 
within-tree distributions and biologies of selected arthropod natural enemies in different states 
(Berisford 1976; Smith 1978; Dixon and Payne 1979a and b; Goyer and Finger 1980); Smith and 
Goyer 1980; Nebeker and Purser 1980). The impacts, roles, and prey preferences of four species of 
avian predators of the SPB in Texas were studied (Kroll and Fleet 1979; Kroll et al. 1980). 
Sikorowski et al. (1979) evaluated SPB mortality from different pathogens and seasonal prevalence 
of SPB pathogens in Mississippi and Alabama. 


In 1980, an exclusion cage for assessing SPB mortality from natural enemies was developed. This 
technique was used to determine the linear relationship between number of SPB eggs per 100 cm of 
gallery and number destroyed per predator (Linit and Stephen 1983). Miller (1984a and b) also used 
an exclusion-interference technique to determine Jps spp. mortality during brood development and 
during different generations. 


Other researchers developed techniques for identifying previous hosts of natural enemies and 
assessing the impact of alternative hosts on natural enemy abundance especially when preferred hosts 
were scarce. Miller and others used immunodiffusion and immunoelectrophoresis techniques to 
produce antisera specific for SPB, black turpentine beetle, and Jps spp. (Miller 1979; Miller et al. 
1979). Kudon and Berisford (1980, 1981) compared free fatty acids in parasites and their bark beetle 
hosts, and studied host preferences. They found that most bark beetle parasites exhibit a strong 
preference for the host species from which they originated and will disperse to search for those hosts 
rather than parasitize a different species. These observations were confirmed in subsequent field 
trials (Kudon and Berisford 1985). 


Post-Expanded SPB Research and Applications Program. Research and application efforts on the 
SPB and its natural enemies for the most part stopped when funding by the ESPBRAP ceased. 
However, a few Forest Service scientists in the Southern Forest Experiment Station continued their 
efforts. Miller et al. (1987) published an overview that discussed the potential for biological control 
of Dendroctonus spp., including the SPB. This publication targeted semiochemicals and insect 
natural enemies of related bark beetles for additional research. Dixon and Payne (1980) identified 
several SPB natural enemies that were attracted to SPB semiochemicals. McGregor and Miller 
(1989) reported the attraction of Thanasimus undatulus, a predator of Douglas-fir beetle, to 
pheromones of SPB and MPB. Miller et al. (1989) studied responses of insect associates of allied 
bark beetle species to aggregation pheromones. 


In 1991, a 30-year record of SPB activity in east Texas was analyzed and it was determined that the 


structure of SPB populations was due to delayed response to density-dependent factors that could 
involve natural enemies and was not due to density-independent factors such as climate (Turchin et 


403 


al. 1991). Also in 1991, scientists at the Forestry Sciences Laboratory in Stoneville, MS, began a 
long-term field study to assess the role of predators on SPB population dynamics. They developed 
cages for excluding predators and determined impacts of decreased predator abundance on SPB 
abundance (Taylor 1991). Study results will improve models describing the population dynamics of 
the SPB and help develop long-term strategies to manage the pest. 


At the same time, John Reeves, a Forest Service entomologist at Pineville, LA, began studies on 
effects of native natural enemies on SPB populations and their pattern of variation during the 
outbreak cycle of the pest. Reeves is measuring the impact of natural enemies on within-tree rate of 
increase in SPB by comparing the increase rates for SPB exposed to natural enemies with those of 
unexposed caged SPB. He then will relate the pattern of variation in natural enemy impact to the 
phase of the SPB outbreak cycle. Reeves also assessed the impacts of adults of the clerid beetle 
Thanasimus dubius on SPB found on and under the tree bark during mass attack, and of 7. dubius 
larvae on SPB immatures within the phloem. Although results of this study have not been published, 
Reeves found that 7. dubius had a much longer than expected development time. This finding could 
have significant implications on SPB management because existing protocol calls for the removal of 
trees that have been vacated by SPB, but which still contain immature 7. dubius (J. Reeves, personal 
communication). 


7. Mites and nematodes as natural enemies of bark beetles. By Donald N. Kinn 


An epidemic of the spruce beetle that began in 1940 and lasted into the mid-1950s ultimately 
destroyed eight billion board-feet of lumber in Colorado, Idaho, and Montana (Massey 1956). 
Research on the biology and control of this pest by personnel of the Rocky Mountain Forest and 
Range Experiment Station began in 1944. Initially, artificial control tactics were employed, but these 
proved to be too expensive. Consequently, studies were initiated in 1950 to determine the feasibility 
of combating this insect using natural control agents. Observations revealed that the galleries of this 
pest were heavily infested with nematodes. C.L. Massey, the only nematologist with the Rocky 
Mountain Forest and Range Experiment Station, was assigned to the Forest Insect Laboratory at 
Albuquerque, NM, which is maintained in cooperation with the University of New Mexico (Massey 
1974). 


Although nematodes had been found associated with the mountain pine beetle and several European 
bark beetles, little was known of the numbers, species, or effect that nematodes have on their host. 
Therefore, the objective of the study was to survey and identify nematode parasites and associates of 
the spruce beetle. Ultimately, four endoparasitic species were found associated with this pest. 
Sphaerulariopsis dendroctoni was found in the body cavity of adult beetles with infestation rates 
ranging as high as 35%. This species is a true parasite and does not kill its host, but it does reduce 
oviposition of infested females by 62%. Contortylenchus reversus and Ektaphelenchus obtusus also 
were found in the body cavity, in immature instars as well as adults. Parasitorhabditis obtusa infests 
the alimentary canal of all instars of the spruce beetle. Contortylenchus reversus, like S. dendroctoni, 
greatly reduces egg production by infected females. The effect of E. obtusus on its host is not known 
and Massey (1956) suggested that P. obtusa has little effect on its host. Thirteen other nematode 
associates of the spruce beetle were collected from the galleries. 


In 1957, studies were initiated on nematode parasites and associates of Ips confusus. This beetle was 
responsible for killing major portions of pinyon pine on 800,000 acres in New Mexico and Arizona 
(Massey 1960a). Three species of endoparasitic nematodes were recovered from the larvae, pupae, 
and adults of J. confusus. One of these internal parasites, Contortylenchus elongatus, reduces the egg- 
laying potential of infected beetles by 50%, but parasitism by this nematode does not result in the 
death of the host. The parasite's life cycle closely parallels that of its host (Massey 1962a). Mating 
occurs in the host gallery and the female parasitizes beetle larvae and pupae. Eggs are deposited in 


404 


the body cavity of the host only after the insect becomes an adult. The earlier in its development that 
an immature beetle is infected, the more pronounced is the reduction in fecundity. The other two 
species of nematodes found internally in 1. confusus, Parasitaphelenchus gallagheri and 
Parasitorhabditis obtusa have little effect on the insect (Massey 1960a). Four additional nematode 
species, including one new species, were recovered from beetle galleries. 


Surveys of nematodes and associates of bark beetles were expanded to include more and more bark 
beetle species. Studies on the nematode parasites and associates of the fir engraver in New Mexico 
revealed two species of internal nematodes (Massey 1964a, 1964b). These species, 
Sulphuretylenchus elongatus and Neoparasitylenchus (as Sulphuretylenchus) scrutillus, are unusual 
in that they first sterilize and then kill their host. Massey (1964a and b) credits these parasites with 
the decline and termination of an infestation at Ruidoso, NM. He speculated that biological 
evaluations predicting the decline of infestations may be based on the short galleries produced by 
infested beetles. In addition to the two parasitic species, 11 other species of nematode associates 
were found with this insect. All were described as new by Massey (1964a and b). 


Furniss (1967) examined populations of the Douglas-fir beetle from Idaho and Utah for nematode 
associates. About 97% of the insects examined were infested with at least one species of nematode. 
Parasitism did not vary significantly between male and female beetles. Furniss speculated that some 
nematode associates of the Douglas-fir beetle may serve as prey for predaceous mites during those 
periods when immature instars of the beetle are not available. 


A recent ecological study of nematode parasites of Jps beetles from California and Idaho revealed 
that infection rates by Contortylenchus spp. and Parasitorhabditis spp. increase in later emerging 
beetles (Choo et al. 1987). 


In the southeastern U.S., Moore (1970a) sprayed the bark of southern pine beetle-infested shortleaf 
pines with Steinernema carpocapsae and a wetting agent and obtained a 44% reduction in brood 
adults. This tactic, if perfected, would probably be practical in high value or wilderness areas only. 
Kard (1991) found no mortality of southern pine beetle larvae that could be attributed to Steinernema 
that were sprayed onto the bark of infested loblolly pine bolts. 


An outbreak of the roundheaded pine beetle in ponderosa pine on the Lincoln National Forest, NM, 
killed over 5000 trees between 1961 and 1965. A survey of nematodes associated with this insect 
revealed 25 species, of which nine were new to science, and two internal parasites, 
Sulphuretylenchus stipatus and Parasitaphelenchus dendroctoni (Massey 1966a). Like other 
nematode parasites of bark beetles, the life cycles of these are closely synchronized with that of their 
host. 


The above studies by Massey and others established that the effect of endoparasitic nematodes on 
their bark beetle hosts generally involve: 1) reduced fertility, 2) delayed emergence, 3) altered 
behavior, 4) reduced flight ability, or 5) possible decreased adult longevity. 


Surveys of nematodes associated with bark beetles throughout the U.S. revealed numerous new 
species (Massey 1957, 1958, 1960b, 1962b, 1963, 1964a and b, 1966b, 1967, 1969, 1971). Massey 
(1962b) suggested that some nematodes of the family Diplogasteridae found under the elytra of bark 
beetles may be predaceous on beetle eggs. However, no experimental evidence of predation exists. A 
rhabditid species observed on dead eggs of the mountain pine beetle was actually feeding on spores 
of a fungus, Beauveria sp., which was responsible for the death of the eggs (D.N. Kinn, unpublished 
data). 


405 


By the time Massey retired from the Forest Service in 1972, he had discovered and described more 
than 55 new species of nematodes associated in one way or another with bark beetles. In his final 
publication (Massey 1974), he described 50 additional new species and illustrated 32 parasites and 
112 nematode associates of bark beetles. 


Massey (1966c) speculated that: 1) the lethal potential of a parasitic nematode might be increased on 
a novel host species of the same or closely related genus, 2) it may some day be possible to mass rear 
nematodes for introduction into bark beetle infestations, 3) the planned introduction of infested 
beetles into a beetle population may result in an increase in the percentage of sterilized beetles, 4) if 
the life cycle of parasitic nematodes could be altered in such a way that they attain maturity in 
immature beetles, their effect would be more pronounced, 5) external symptoms exhibited by 
nematode-infected beetles may be used to predict pest population trends, and 6) nematodes are 
excellent candidates for integrated control strategies because many kinds of insecticides have no 
effect on them when applied as water emulsions against host beetles. 


In 1952, forest entomologists employed with the BEPQ were transferred to the U.S. Forest Service 
Division of Forest Insect Research (FIR). At the request of the Texas Forest Pest Action Committee, 
the Southern Forest Experiment Station assigned one entomologist, R.E. Lee III, to southern pine 
beetle (SPB) research, locating him first in Liberty and then in Nacogdoches, TX. In 1955, Lee was 
replaced by R.C. Thatcher. In the same year, the Southern Forest Experiment Station formed a team 
of three entomologists responsible for aerial detection, evaluation and control activities associated 
with SPB and other major bark beetle pests. 


In 1959, Thatcher prepared a project analysis titled "The Southern Pine Bark Beetles" in which he 
reviewed the literature and outlined general research needs for the five bark beetle species that attack 
southern pines. This document was revised and published as a Southern Forest Experiment Station 
Occasional Paper (Thatcher 1960). One of the recognized needs cited in this paper was research into 
chemical, biological and silvicultural means of dealing with bark beetles. It was also noted that lack 
of basic information was a handicap to applied research. This analysis, and the formation of a State 
and Private Forest Pest Management Division in Region 8, led to the formation of a Forest Insect 
Research Unit at Pineville, near Alexandria, LA, with W.H. Bennett as Project Leader. The original 
mandate charged to this unit was to investigate the biology and control of the SPB, black turpentine 
beetle (BTB), and other bark beetles. Early research undertaken by the unit was to improve chemical 
formulations and techniques for bark beetle control. With the transfer of J.C. Moser into the unit in 
late 1962, research on the natural enemies of these bark beetles began. Moser, the first of eventually 
six research scientists, and Bennett initiated studies on insect and acarine associates of the SPB and 
other bark beetles during the first year of the unit's existence. Research on mite associates involved 
two cooperative research grants, one with H.B. Boudreaux, Louisiana State University, Baton Rouge, 
and the other with E.A. Cross, then at Northwestern State College, Natchitoches, LA. Contact was 
made with numerous mite taxonomists throughout the world to aid in species identifications and 
descriptions. Entomologists within the Forest Service and several entomologists outside the U.S. 
were contacted with the aim of finding acarine enemies of other bark beetles that might be more 
effective than native mites in maintaining the SPB at endemic levels. By 1964, more than 700 mite 
specimens had been collected from various bark beetles and distributed to ten taxonomists for 
identification. This initial survey revealed 26 new species of mites distributed among 12 families. 
Partial life histories of four possible natural control agents were determined. These species, new to 
science at that time, were Macrocheles boudreauxi, Schizosthetus lyriformis (= Eugamasus 
lyriformis), Trichouropoda australis, and Siteroptes bennetti (= Pygmephorus bennetti). None of 
these species were observed to feed on any instar of the SPB. Macrocheles boudreauxi fed on other 
mites, S. lyriformis fed on other mites and nematodes, and both T. australis and S. bennetti appeared 
to feed on fungi. Upon completion of these and other studies, an addendum to Thatcher's project 


406 


analysis listing known insect and mite associates of bark beetles of southern pines and the possible 
roles of these associates was prepared by Moser and L.S. Pickard in 1964. 


With urging from the Texas Forest Service, the Director of the Southern Forest Experiment Station 
decided the unit should take an entirely different approach to bark beetle research. Therefore, 
beginning in late 1962 additional funds were provided to increase its staff to six scientists working as 
a team to develop silvicultural and biological control of the SPB in relation to its environment and 
describe the causes of epidemics. At that time, felling and spraying infested trees with chemicals was 
the only method used to control infestations. The goal of the newly formed unit was to develop 
silvicultural and biological measures that prevent rather than control outbreaks. Most, but not all, the 
research undertaken by members of the unit was conducted on the Kisatchie National Forest, LA, and 
the pine species most often studied were loblolly and shortleaf pine. 


Surveys of mites associated with bark beetle-attacked trees revealed many species previously 
unknown to science (Woodring 1963, 1966; Hunter and Moser 1968; Smiley and Moser, 1968, 1970; 
Woodring and Moser 1970) some of which are only passively associated with bark beetles. 
Observations on the biology of some of these species were published (Woodring 1969) and keys 
prepared for selected groups of mites (McGraw and Farrier 1969; Kinn 1976). Throughout the 
duration of these studies, new mite species and heteromorphic forms of known species continued to 
be discovered (Cross and Moser 1971; Smiley and Moser 1974, 1975, 1984a and b, 1985; Hunter et 
al. 1989). Many of these species are inhabitants of pine bark but others are parasitic on bark beetles 
(Moser 1979; Moser and Vercammen-Grandjean 1979; Cross et al. 1981). Sampling methods were 
improved (Kinn 1979), phoretic preferences in site of attachment to their hosts and attachment times 
observed (Roton 1978), and seasonal and spatial fluctuations in populations of mite associates noted 
(Kinn 1982; Stephen and Kinn 1980). 


In 1966, Bennett wrote the unit's first problem analysis. The approach to solving the SPB problem 
was divided into three areas: insect biology and physiology, site and host-physiological relationships, 
and bark beetle associates. The latter included a continuation of research on mite associates and 
proposed research on nematode associates. By this time about 100 species of mites had been found 
associated with trees infested by one or more of the five bark beetles of southern pines (Moser and 
Roton 1971). Most of these species seemed to feed on other mites or bluestain fungi. However, 
several natural enemies of bark beetles, other than SPB, were found. Eight species were suspected to 
feed on SPB (Moser 1975). 


The first formal Research Work Unit (RWU) Description was prepared by Bennett in 1971. The 
study areas proposed were divided into three phases: the mensurational phase, the ecological phase, 
and the management phase. The ultimate goal of the research was to coordinate silvicultural and 
biological techniques with other promising control measures. Research on natural control agents, 
primarily mites, continued to be supported by base funding of the unit. Revisions of the RWU 
Description approved in 1978 and 1982 continued to include studies on mites and nematodes as 
natural control agents of the SPB. 


In 1974, the USDA Combined Forest Pest Research and Development Program (CFRP) was 
established and the six year Expanded SPB Research and Applications Program (ESPBRAP) funded. 
Although natural and biological control studies were given a low priority, a few such studies were 
funded. Studies on the natural control of SPB by mites and nematodes by Moser were funded by 
ESPBRAP for two years. This enabled the unit to add another full time employee to work on 
biological control. D.N. Kinn joined the unit in 1975 and was assigned the task of verifying the 
feeding habits and life histories of those mites that appeared to be natural control agents. His duties 
were later expanded to include the impact of endoparasitic nematodes on SPB populations. Several 
other studies outside the Forest Service were also funded by ESPBRAP. These included those by P.P. 


407 


Sikorowski (Mississippi State University) and G.E. Allen (University of Florida) who investigated 
the impact of pathogens on SPB, and by V.G. Perry and R.C. Wilkinson (University of Florida) who 
investigated the impact of endoparasitic nematodes on SPB. 


The life cycles of three of the most common mesostigmatid mites associated with SPB were 
determined (Kinn and Witcosky 1977; Kinn 1983, 1984a). All active instars of these species fed on 
nematodes, including the free-living instars of endoparasitic nematodes. The relationship of these 
mites with their bark beetle hosts appears to be one of phoresis and mutualism (Kinn 1980). Bark 
beetles provide the means by which the flightless mites are transported to new beetle infestations, 
and the beetles may benefit from reduced nematode parasitism due to the feeding activity of the 
mites. However, the presence of phoretic mites appears to adversely affect beetle flight (Kinn and 
Witcosky 1978). 


Numerous disease agents were found in SPB populations (Knell and Allen 1978; Pabst and 
Sikorowski 1980) causing an average mortality of 22% over a 2-year study period (Sikorowski et al. 
1979). A microsporidan was found to be prevalent in endemic SPB populations but scarce in 
epidemic populations (Bridges 1987). The incidence of endoparasitic nematodes (Contortylenchus 
spp.) was found to be as high as 24% in some populations (Joye and Perry 1976) and one species, C. 
brevicomi, reduced beetle fecundity (MacGuidwin et al. 1980). In addition, there was evidence that 
endoparasitic nematodes may alter the flight capabilities or host finding behavior of infected SPB 
(Atkinson and Wilkinson 1979; Kinn and Stephen 1981). The flight behavior of female engraver 
beetles also appears to be altered by endoparasitic nematodes (Kinn 1984b). By 1981, a total of 16 
papers reporting research on microorganisms, nematodes, and mites, funded in total or part by 
ESPBRAP, were published. 


In the 1978 RWU Description, it was recognized that the SPB is intimately associated with a large 
number of other organisms and that an understanding of the life processes of the pest and its 
associates was essential if models that forecast population trends were to be developed along with 
control strategies to augment beetle population suppression by natural enemies. 


The concept of "new associations" (Pimentel 1963) was applied to mites preying on bark beetles. 
Pyemotes giganticus, an egg parasite of the "Douglas-fir pole beetle" (Pseudohylesinus nebulosus), 
was imported from the western U.S. and studied as a possible extraregional parasite of the SPB 
(Moser 1981). Although this mite readily attacks beetle eggs in the laboratory, it parasitizes less than 
1 percent of bark beetle eggs in the field. Therefore, this species was never released in the south for 
SPB control. Life histories of several other pyemotid mites were also determined. Pyemotes 
parviscolyti attacks all immature instars of Pityophthorus annectens (as P. bisulcatus) in the field, 
but never comes in contact with economically important bark beetles (Moser et al. 1971a). A 
European species, Pyemotes dryas, was found to feed on SPB under laboratory conditions, but would 
not become phoretic on any North American bark beetle and is thus a non-viable candidate for 
biological control of North American bark beetles (Moser et al. 1978). 


An ecological paper (Wilson 1980) based on data gathered by Forest Service personnel theorized that 
mite species closely associated with their host would be less efficient control agents than those not 
dependent upon the host for transport. With the realization that the most common mite associates of 
the SPB may be beneficial rather than detrimental to beetle populations, research was undertaken to 
clarify the relationships existing among the various mite and nematode species present in the 
subcortical habitat and the role of various microorganisms in the ecology of bark beetles. 


Tarsonemid mites were found to vector the bluestain fungus, Ceratocystiopsis ranaculosus (Bridges 
and Moser 1983, 1986; Moser 1985; Moser and Bridges 1986), which can be detrimental to SPB 


development. Methods were developed to rear bark beetles free of mites (Moser and Bridges 1983; 


408 


Kinn and Roton 1988). Because the unit was known for its expertise on mites, numerous mite species 
collected from forest pests throughout the world were first sent to the Pineville, LA, laboratory and 
then forwarded to various taxonomic experts. Among these mites was Pyemotes barbara, a potential 
natural control agent of cone and seed insects (Moser et al. 1987). 


In anew RWU Description in 1987, research on mites, nematodes and microorganisms was phased 
out of the unit's mission and in 1989 Moser retired. Research on mites and nematodes conducted at 
the Pineville, LA, laboratory had led to the realization that not only do some of these organisms prey 
on or parasitize bark beetles but others have potential as indices for predicting pest population trends. 


Not all research on biological control of the SPB was conducted at the Pineville laboratory, and not 
all biological control research was aimed at controlling this pest. At the Southern Forest Experiment 
Station at Gulfport, MS, Kard (1991) studied the possibility of controlling SPB larvae using 
steinernematid nematodes. Although laboratory tests were very successful, field trials were 
disappointing. Earlier field studies conducted out of the Southeastern Forest Experiment Station 
revealed that successful survival of Steinernema carpocapsae was dependent upon moist 
environments or a relative humidity above 90% (Moore 1970a, 1973a). Steinernematid nematodes 
have also been reported as potential control agents of other forest pests (Schmiege 1963; Moore 
1973a). 


Before the creation of a Forest Insect Work Unit in Louisiana, mites had been noted as associates of 
bark beetles and were suspected of being natural enemies of these pests. DeLeon (1930) in an 
unpublished report noted that nematodes and mites were often associated with the mountain pine 
beetle (MPB), and in other unpublished reports Bedard (1932, 1933a) noted that two unidentified 
mite species fed on the eggs of the Douglas-fir beetle under laboratory conditions. Rust (1933) 
reported up to 85% of pine engraver (as Jps oregonis) eggs destroyed by mites. In the Pacific 
Southwest, Lindquist and Bedard (1961) reported on the biology and taxonomy of Tarsonemoides (as 
Iponemus) species parasitizing eggs of Jps engraver beetles. Beal (1965) credited nematodes with 
terminating a fir engraver outbreak in New Mexico and mites, along with insect parasitoids, as 
playing major roles in stopping a SPB outbreak in Texas. Boss and Thatcher (1970) studied mites 
associated with Dendroctonus and Ips species in the Rocky Mountain region. Although no mites 
were found to attack Dendroctonus species, a Dendrolaelaps sp. preyed upon eggs of numerous Jps 
species, and mites of the genus Jponemus selectively parasitized eggs of Ips beetles. 


B. Shoot and Trunk Borers and Sheathminers. By Mary Ellen Dix and Shivanand Hiremath 
1. Shoot borers and sheathminers (Lepidoptera: Tortricidae and Yponomeutidae) 


In 1915, entomologists of the Bureau of Entomology's Division of Forest Insects' Gypsy Moth 
Laboratory in Melrose Highlands, MA, initiated a long-term study to identify lepidopterous insect 
pests and their parasites in the northeastern U.S. This study focused on rearing field-collected 
lepidopteran larvae and documenting their distribution and food preferences. The entomologists also 
identified all emerging parasites and documented aspects of their life cycles. R.C. Brown 
(Entomologist-in-Charge of the Bureau's Division of Forest Insect Investigations, New Haven, CT) 
encouraged the entomologists to collect extensively and rear microlepidopteran tree pests, such as 
shoot borers (Rhyacionia spp., Retinia spp., and Petrova spp.) and sheathminers (Taniva spp., and 
Zelleria spp.). These early studies provided information on the identity and distribution of the tree 
pests and their parasites. Such data often were the earliest available information on the species and 
have been an invaluable resource for later forest entomologists. When the USDA reorganized in the 
early 1950s, these records were transferred to the Northeastern Forest Experiment Station of the 
Forest Service. J.V. Schaffner, Jr., summarized the results of the microlepidoptera study in 1959. 
(Results of the similar study of macrolepidoptera and their parasites was published by the Bureau of 


409 


Entomology in 1934 [Schaffner and Griswold 1934]. Other research on biologies and releases of 
parasites of forest insects by USDA entomologists prior to 1953 is discussed in Chapters I and II 
above.) 


During the 1960s and 1970s, Forest Service entomologists continued to identify natural enemies of 
shoot borers and other microlepidoptera, and to describe their biologies (e.g.: Yates 1960, in Georgia; 
Miller et al. 1961, in Minnesota; Stevens 1966, 1971, in California; Torgersen and Coppel 1969, in 
Wisconsin; Koerber and Struble 1971, in California; Yates and Beal 1971, in Georgia; Brewer and 
Stevens 1973, in Colorado; McKnight 1973, in Colorado; Jennings 1975, in New Mexico; and Yates 
et al. 1981, in Georgia). Shoot and tip borers of the genus Rhyacionia received considerable attention 
at all Forest Experiment Stations in the U.S. (Yates 1967a and b). However, except for the European 
pine shoot moth and the Nantucket pine tip moth, most studies were short-term and focused on pests 
of local or regional importance. A more detailed discussion of these studies follows. By 1967, 
entomologists had identified over 100 species of parasites of Rhyacionia. Yates (1967b) reviewed 
published papers on the genus Rhyacionia and developed a key to both native and introduced 
Rhyacionia parasites. This key also contained notes on parasite biologies and introductions, and 
listed relevant publications. 


European pine shoot moth, Rhyacionia buoliana (Denis & Schiffermiiller). This moth is an 
introduced insect that damages the buds and shoots of pines. The moth was discovered on Long 
Island, NY, in 1913 and by 1915 had spread to Ohio (Miller and Neiswander 1955). By 1958, the 
borer was found in red pine plantations from eastern Canada and northeastern U.S. south to Virginia, 
and as far west as Wisconsin and Michigan (Torgersen and Coppel 1965). In the late 1960s, the shoot 
moth was discovered in pine plantations, in Christmas trees and in planted trees in residential areas 
around Puget Sound in Washington (Ryan and Medley 1970). 


Parasites of this shoot moth have been introduced into the U.S. and Canada to control outbreaks of 
the pest since 1928 (Dowden 1962; McGugan and Coppel 1962a). Over 700,000 individuals 
representing more than 16 species were introduced between 1928 and 1958 (Dowden 1962; Miller 
1967). In Michigan and Ohio alone, about 16,000 parasites were released between 1959 and 1962 
(Miller 1967). However, these releases were considered to be failures because of poor parasite 
survival and lack of long-term moth control (Arthur and Juillet 1961; Turnbull and Chant 1961; 
Miller 1967). Arthur and Juillet (1961) speculated that unfavorable release conditions reduced 
parasite survival and chance of establishment. 


During the 1950s and 1960s, Forest Service and university entomologists initiated a series of studies 
to learn more about parasite complexes in Ohio, Wisconsin, Michigan, and Washington. These 
scientists investigated parasite bionomics, impacts, and biologies (Miller and Neiswander 1955; 
Miller 1959; Torgersen and Coppel 1965). They discovered that in spite of the massive earlier 
introductions, parasite populations were lower in North America than in Europe. The European 
braconid parasite Orgilus obscurator was, however, discovered to be established at several sites in 
Michigan after an earlier release in Ontario (Miller 1970). 


During the 1960s and 1970s, studies were initiated under Public Law 480 (PL-480) with cooperators 
in Yugoslavia, Poland, India and other countries to identify potential parasites for importation and 
release in the U.S. The PL-480 scientists inventoried parasites, assessed their impacts, developed 
rearing techniques, identified alternative hosts, and obtained other needed information to accelerate 
parasite releases and enhance their establishment in the U.S. (Koehler and Kolk 1969; Vasic 1972; 
Rao and Chacko 1972; Forest Service Annual Reports). 


In 1969, 5,365 female Jtoplectis quadricingulata were released on a 40-acre site in western 
Washington to suppress populations of R. buoliana (Ryan and Medley 1970). The Forestry Sciences 


410 


Laboratory in Corvallis, OR, mass-reared this ichneumonid parasite prior to release. The parasite 
infested about 30% of the shoot moth larvae and about 50% of the stocked cohorts of the greater wax 
moth larvae at the site. Ryan and Medley (1970) concluded that the host-tree shoots and buds 
surrounding the shoot moth larvae probably protected them and hampered parasitism. However, they 
felt that host preferences and searching behavior of the parasite needed to be more fully understood 
before the parasite could be recommended for control of the European pine shoot moth. 


Nantucket and western pine tip moths, Rhyacionia frustrana (Comstock) and R. bushnelli Busck, and 
southwestern pine tip moth, R. neomexicana (Dyar). In the late 1800s, the Nantucket pine tip moth 
(NPTM) was discovered in New England. This tortricid is now distributed from southern New 
England to Florida and west to eastern Nebraska and Texas. The larvae mine the buds and new 
growth of young trees in pine and Christmas tree plantings, thereby stunting growth and killing the 
trees. The western pine tip moth (WPTM) damages native and planted ponderosa, red, jack and 
Scotch pines in Montana, the Dakotas, Nebraska, Arizona and New Mexico (Powell and Miller 
1978). Daniel T. Jennings (1975), an entomologist with the Rocky Mountain Forest and Range 
Experiment Station in Albuquerque, NM, identified parasites and predators of the southwestern pine 
tip moth, and assessed the impact of spiders and other predators on its abundance. 


Numerous researchers have identified natural enemies of NPTM and WPTM (Cushman 1927a and b; 
Yates 1960, 1966, 1967a and b; Eikenbary and Fox 1968; Nash and Fox 1969; Dick and Thompson 
1971; McKnight 1973; J.E. Pasek unpublished data). Yates (1967a) developed an X-ray technique 
for detecting parasites in concealed tip moth larvae. He also identified diagnostic characteristics for 
the interpretation of radiographs of shoot tips containing Rhyacionia spp. and their parasites and 
predators. This technique permitted the selective rearing of tip moths and their parasites without the 
destruction of their microenvironment. 


The most famous release of NPTM parasites occurred in Nebraska. Between 1902 and 1909, the 
WPTM immigrated into young ponderosa pine plantations in the Nebraska National Forest. By the 
early 1920s, pines in this man-made forest were severely damaged by WPTM. In 1924, Cushman and 
other Bureau of Entomology (BE) entomologists identified parasites of NPTM that might be useful 
for control of WPTM in Nebraska (Cushman 1927a and b). The next year, pine tips infested with 
parasitized NPTM from Virginia were sent to Nebraska where L.G. Baumhofer, an entomologist 
assigned by the BE to control the outbreak, reared and released the parasites. In 1926, the process 
was repeated with tips collected in both Virginia and Massachusetts (Graham and Baumhofer 1927). 
Nine species of parasites were released in 1925; 11 species were released in 1926 (Dowden 1962). In 
1927, Graham and Baumhofer identified the parasites of WPTM in the Nebraska National Forest and 
described their biologies. One parasite, the ichneumonid Campoplex frustranae became established 
and controlled the WPTM within five years. Survival of the other parasite species was poor (Dowden 
1962). During the 1930s, southwestern pine tip moth abundance increased rapidly in the forest and it 
became the primary pest there. Campoplex frustranae did not parasitize this species. 


Melvin E. McKnight of the Rocky Mountain Forest and Range Experiment Station (RM) location at 
Bottineau, ND, reared WPTM and NPTM from infested shoots collected throughout the Great Plains. 
He reared C. frustranae from samples collected in the Nebraska National Forest, De Smet, SD, and in 
western North Dakota (McKnight 1973; Unpublished data, RM, Lincoln, NE). During the mid-1980s, 
Judy Pasek (RM, Lincoln, NE) reared and identified tip moth parasites, while evaluating the impact 
and seasonal activity of WPTM and NPTM in eastern Nebraska (J.E. Pasek, unpublished data). In the 
early 1990s, Carol Bell (Forest Pest Management, Region 1, Missoula, MT) identified natural 
enemies of Rhyacionia spp. as part of her M.S. research to evaluate abundance, distribution, and 
impact of shoot borers in the western Dakotas and eastern Montana (C. Bell, unpublished data). 


41] 


Nash and Fox (1969) applied the nematode DD-136 (Neoaplectana carpocapsae) to NPTM-infested 
pines. The nematode killed more first generation larvae than second or third generation larvae. 
Subsequent use of the nematode was not recommended because survival of the nematode was poor 
(Nash and Fox 1969). 


Other shoot borers and sheathminers. In the western U.S., a series of short-term regional studies was 
initiated on the biologies and impacts of natural enemies of several species of shoot borers and 
sheathminers. R.E. Stevens (1966, 1971), of the Pacific Southwest Forest Experiment Station (PSW), 
identified natural enemies of the "ponderosa pine tip moth", Rhyacionia zozana, in California. Later, 
Niwa (1988), of the Pacific Northwest Forest Experiment Station (PNW), re-examined R. zozana 
populations in California and Oregon, and identified their natural controls and assessed their impacts 
on moth abundance. Stevens later transferred to the Rocky Mountain Forest and Range Experiment 
Station (RM) in Fort Collins, CO, where he studied the biologies and identified the parasites of the 
pine needle sheathminer and "pinyon pitch nodule moth", Petrova arizonensis (Stevens 1971; Brewer 
and Stevens 1973). 


Larvae of the "metallic pitch nodule moth", Retinia metallica, mine the growing tips of ponderosa 
and other pines in the Great Plains; such mining stunts and deforms the trees (Dix et al. 1987). In 
1986, Mary E. Dix, of the RM station at Lincoln, NE, began a study to identify and assess the impact 
of natural enemies on abundance of R. metallica in pine windbreaks. The identities, impacts, and 
biologies of parasites were determined through rearing trials and field observations. Dix also 
identified potential predators on branches and documented their seasonal abundance. She found that 
spiders were the most abundant predator on the trees and that their abundance was influenced by the 
surrounding vegetation (Dix 1991b; unpublished data). In cooperation with entomologists and 
wildlife biologists from the University of Nebraska, Dix currently (1993) is assessing the impact of 
vegetative diversity and agroecosystem management practices on predator abundance in tree-crop 
and tree-turf ecosystems. Results of this research will be used to develop techniques for increasing 
survival of natural enemies of tree pests. By manipulating ecosystem diversity and by modifying 
agriculture and turf management practices, natural enemy effectiveness may be enhanced. 


Predators. Spiders are among the most abundant arthropod predators found on trees. Population 
densities of arboreal spiders are estimated to exceed 645,000 spiders/hectare (Jennings and Collins 
1987). However, despite their ubiquitous occurrence and predatory habits, few studies have 
addressed the importance of spiders in forest ecosystems. Unless spiders are actually observed 
feeding on their prey, or "stock" their prey in webs, it is difficult to determine their diets, prey 
preferences, and impacts on target forest pests. Consequently, information on the roles spiders play 
in maintaining and regulating forest pests of pine is very limited. During the 1970s, Jennings (RM, 
Albuquerque, NM) collected, identified, and described habitat preferences of spiders found on pines 
and other trees in New Mexico, Colorado, Texas, Nebraska, South Dakota, and Wisconsin (Jennings 
1972, 1981; Jennings and Toliver 1976; Cutler et al. 1977; Cokendolpher et al. 1979; Jennings et al. 
1989). He found that crab and lynx spiders were common on pines and in pine-juniper ecosystems 
(Jennings 1974, 1981; Jennings and Toliver 1976; Cutler et al. 1977). Crab spiders were observed 
feeding on the pine butterfly (Jennings and Toliver 1976), on scarab beetles (Jennings 1974) and on 
southwestern pine tip moth (Jennings 1975; Lawson et al. 1983). 


Most studies have concerned the identification of all spider species associated with a defined 
ecosystem or on tree species (Jennings 1972, 1974; Jennings and Dimond 1988; Cokendolpher et al. 
1979; Jennings et al. 1989, 1990a and b; C.L. Griswold, unpublished data). Related observations 
have been made on spider biologies, feeding behaviors, and prey (Jennings and Toliver 1976; Cutler 
et al. 1977; McDaniel and Jennings 1983; Hayes and Lockley 1990). Spiders in spruce and fir were 
identified by Hilburn and Jennings (1988) and Jennings et al. (1990a), but little else is known about 
natural enemies of shoot borers in spruce-fir forests. In Nebraska, Dix (unpublished data) collected 


412 


information on the identity, distribution and impact of spiders on Retinia metallica population 
dynamics. She also has documented the distribution of spiders in tree-crop and tree-turf landscapes. 


Many species of spiders are usually highly mobile, nocturnal, and secretive in their behavior; 
consequently, it is extremely difficult to assess their effectiveness in regulating prey populations. 
Three general approaches to evaluation of spider effectiveness have been developed: 1) direct 
observations and assessment of hunting spiders with and without prey; 2) direct observations of web- 
spinners and their catches, including "stocked" prey in webs; and 3) indirect assessment of predation 
on target insects by immunological assays. Hayes and Lockley (1990) observed the nocturnal feeding 
behavior of wolf spiders in cotton fields on Coleoptera and Diptera. They found that prey selection 
and temporal activities showed a distinct separation by species and developmental stage. 


2. Trunk borers 


Boring insects tunnel through the wood, killing or severely weakening, and degrading lumber of 
infested trees. They tend to have few natural enemies because they are protected within their host 
tree for most of their life cycles and are difficult to detect. Available information on natural enemies 
is obtained through direct observation of their feeding or searching behavior or by rearing the borer 
larvae. During the 1970s and 1980s, James D. Solomon, of the Southern Forest Experiment Station 
(SO), Stoneville, MS, identified parasites, predators, and pathogens of the carpenterworm, clearwing 
moths, and other hardwood borers in Mississippi. Solomon and Toole (1968) also observed 
carpenterworm pupae trapped in galleries by fungal mycelia. McKnight and Tagestad (1972) (RM, 
Bottineau, ND)) and Dix (unpublished) (RM, Lincoln, NE) identified parasites reared from the 
carpenterworm and lilac borer, respectively, in the Great Plains, and observed bird predation on adult 
carpenterworms (unpublished data, RM, Lincoln, NE). 


Woodpeckers can destroy large numbers of overwintering trunk borer larvae. Woodpecker predation 
on several species of hardwood borers was reported in Ohio and Mississippi (Solomon 1969; Hay 
1972; Galford 1985) and on longhorned beetles in California firs (Wickman 1965). 


3. Root borers 


Phyllophaga spp. larvae (June beetles or white grubs), are widely distributed in the U.S. and other 
parts of the world. While generally considered an agricultural pest of field crops and turf, the grubs 
injure the roots of nursery seedlings, newly transplanted saplings, trees and ornamentals by chewing 
off or girdling the roots (Wilson 1977). White grubs can become a major pests on economically 
important pine and fir seedlings (Stone and Schwartz 1943; Shenfelt et al. 1954; Fowler and Wilson 
1971, 1975; Sutton 1975; Fowler et al. 1982; Bruhn and Heyd 1986; Kard and Hain 1987a and b, 
1988; Mitchell et al. 1992). Damaged seedlings have inadequate nutrient uptake and support, and are 
predisposed to various soilborne fungal pathogens, such as species of Fusarium, leading to the death 
of the seedlings. The consequence is a sparsely populated pine plantation that needs to be replanted 
at a great expense. 


Traditionally, whenever threshold levels of white grub infestations were predicted, chemicals such as 
aldrin and chlordane were used to prepare the soil before planting the seedlings (Fowler and Wilson 
1975, 1982; Kard and Hain 1988; Baxendale et al. 1992). While these methods were usually 
effective, they often resulted in cost overruns and were environmentally unsafe for humans and other 
animals. Although management practices can be used to reduce the mortality of the seedlings from 
white grub damage, plant vigor and overall plantation productivity is reduced. 


In recent years, several different approaches were evaluated for control of white grubs (McLeod et al. 
1986; Kard and Hain 1987b; Kard et al. 1988). Entomopathogenic nematodes were used as a part of 


413 


an IPM program to control white grubs (Kard et al. 1988; Forschler and Gardner 1991; Redmond and 
Georgis 1991). Similarly efforts with entomopathogenic fungi such as Verticillium lecanii (Gour and 
Dabi 1988), Beauveria bassiana and Metarhizium anisopliae (Poprawski and Yile 1990) had limited 
or no impact. Poprawski and Yile (1990) isolated a iridescent virus strain from grubs of Phyllophaga 
anxia. Although injection of this virus into white grubs caused mortality, it was ineffective under 
field conditions. All of the above approaches were ineffective in controlling the white grubs. 


Scientists at Delaware, OH, are using genetically-engineered ectomycorrhizal fungi (EMF) to 
develop species-specific methods that can be easily integrated into other control methods. These 
transgenic EMF alter the microclimate around the conifer roots and produce nutrients and protectants 
that protect the young pines. Advantages of transgenic EMF over other methods of chemical and 
biological control methods include the ability to form a protective mantle around the roots and 
increased environmental safety through use of symbiosis specific promoters. 


Strains of the fungi Laccaria bicolor and Paxillus involutus were isolated from red pine plantations 
and found to be very effective colonizers of several pine species (Richter and Bruhn 1989, 1990, 
1993). A particle gun-mediated transformation system was developed for these strains and 
successfully used to insert genes into these fungi for Hygromycin resistance (selectable marker), beta 
glucuronidase (GUS, reporter gene; useful for tracking transgenic EMFs), and a gene encoding 
BtCrylIIIA, an insecticidal crystal protein (ICP) from Bacillus thuringiensis (Bt). These inserted 
genes were stably integrated and functioning properly in transformed L. bicolor and P. involutus. 


The presence and expression of GUS gene in the seedlings was tested by a modified microfuge tube 
procedure of Roberts et al. (1989). Mycorrhizal synthesis experiments showed that the transgenic 
EMFs retained their ability to form a mycorrhizal mantle around pine roots, expressed GUS, and thus 
provide protection against root pests like white grubs. However, the CrylIIIA protein was not very 
effective on Phyllophaga anxia, but was effective on elm leaf beetle larvae. Bioassays with 
transformants already developed are using elm leaf beetle or other susceptible species to determine 
the efficacy of expression of Bt genes in EMF. The research unit in Delaware, OH, plans to use these 
techniques to introduce Bt genes from the Bt strain Buibui and other strains which are effective 
against scarabs. These techniques can be integrated with other traditional control methods for white 
grubs and also has the potential for biological control of bacterial/fungal pathogens of trees. 


C. Hardwood Defoliators 


1. Cottonwood leaf beetle (Chrysomela scripta Fabricius) and other chrysomelid beetles 
(Coleoptera). By Leah S. Bauer and Mary Ellen Dix 


The cottonwood leaf beetle (CLB) is a native defoliator of Populus spp. throughout North America. 
The larvae and adults are most damaging to newly established plantings of cottonwoods and hybrid 
poplar. The beetles may complete up to seven generations per year in the southern U.S., where 
conventional pesticides are frequently used for their suppression. 


In Mississippi, adults and larvae of the coccinellid Coleomegilla maculata feed on the eggs and 
larvae of CLB. In 1979, Neel and Solomon (Southern Forest Experiment Station [SO], Stoneville, 
MS) initiated a study designed to augument C. maculata abundance in young poplar plantations in 
Mississippi. In March of 1979 and 1980, they collected adult C. maculata at their aggregation sites 
and released them in young cottonwood plantations. The release was of limited success, because C. 


maculata were recovered from the trees for fewer than 14 days after their release (Neel and Solomon 
1985; Solomon and Neel 1985). 


414 


During the 1980s and 1990s, isolates of Bacillus thuringiensis (Bt) were discovered that were toxic 
to some coleopterans. In 1988, Bauer (North Central Forest Experiment Station [NCFES], East 
Lansing, MI) initiated studies to identify Bt isolates with activity against the CLB (Bauer 1990; D. 
Bradley and M. Harkey [University of Washington, Seattle], K.D. Biever [ARS, Yakima, WA], L.S. 
Bauer, and M.-K. Kim [Chonbuk National University, Seoul, Republic of Korea], unpublished data), 
and the imported willow leaf beetle, an exotic pest of poplar and willow (Bauer 1992). Bauer 
conducted field trials with formulated Bt-based insecticides, determined the impact of Bt on leaf 
beetles, and described the ultrastructural damage caused by Bt CrylIIIA toxin on the CLB midgut cells 
(Bauer and Pankratz 1992; Koller et al. 1992). Since 1989, a population of CLB has been selected 
with Bt CrylIJA toxin and high resistance (>1000 times) to the toxin has evolved. In 1992, studies 
were initiated to understand mechanisms of Bt resistance in both CLB and Colorado potato beetles. 
Resistant populations are also being evaluated for cross-resistance to other Bt toxins. The results of 
this research are critical to the development of resistance management strategies for transgenic plants 
that contain Bt toxin genes (Bauer, unpublished data). Research on resistance to Bt is being 
conducted in cooperation with C. Noah Koller, Robert M. Hollingworth, and Mark E. Whalon at the 
Pesticide Research Center, Michigan State University, East Lansing, with funding by the USDA 
Competitive Grants Program. 


No indigenous pathogen was known from CLB despite extensive life table studies, until Bauer 
discovered a microsporidan from CLB collected near Ames, IA. This newly described microsporidan, 
Nosema scripta (Bauer and Pankratz 1993), may be an important natural control factor of CLB, 
although the geographical extent of this pathogen throughout the range of CLB is not known. 
Nosema scripta is transovarially transmitted, and infected beetles die in the egg or larval stages. 
Beetles that survive to the adult stage are smaller, lay fewer eggs, and die sooner than their 
uninfected counterparts. Bauer described the pathology and taxonomic status of N. scripta using light 
and electron microscopy, and studied cross-infectivity with two other chrysomelid species. 


2. Elm spanworm, Ennomos subsignaria (Hibner) (Lepidoptera: Geometridae). By Mary Ellen Dix 


The elm spanworm is a serious lepidopteran defoliator of many broadleaved tree species, particularly 
oaks, hickories, black walnut, and red maple (Drooz 1980; Drooz et al. 1976). Davis (1960) 
identified parasites of the elm spanworm in Georgia. A decade-long outbreak collapsed in 1964 
primarily because of an egg parasite, initially identified as Telenomus alsophilae (Ciesla 1963, 1964; 
Drooz 1964), but which was later shown to be a new species, Telenomus droozi (Drooz et al. 1976; 
Muesebeck 1978). The apparent success of 7. droozi in controlling the elm spanworm and the 
success of 7. alsophilae against the fall cankerworm (see below) spurred an effort to culture both 
species of parasites on other hosts because elm spanworm were difficult to rear. A geometrid, 
Eutrapela clemataria, was selected for mass rearing T. alsophilae (Fedde et al. 1976, 1982). 
Attempts to rear 7. droozi were not successful. 


In 1973, a second species of egg parasite, Ooencyrtus ennomophagus, ended an elm spanworm 
outbreak in Connecticut. Drooz and Solomon (1980) reported that the parasite could be cultured on 
eggs of the poplar tentmaker, but parasite yield from tentmaker eggs decreased with time. Subsequent 
research by Arnold T. Drooz, an entomologist with the Southeastern Forest Experiment Station (SE) 
in Research Triangle Park, NC, and colleagues determined that the parasite could be reared on 
chilled E. clemataria eggs and that cold storage of the eggs did not decrease parasite yields (Drooz 
and Weems 1982; Drooz and Barham 1985). 


In the early 1980s, research on elm spanworm and other defoliators by Drooz, G.F. and V.H. Fedde 


and other SE entomologists ceased because of program redirection. Drooz was transferred to Olustee, 
FL, and the Feddes resigned. 


415 


3. Fall cankerworm, Alsophila pometaria (Harris) (Lepidoptera: Geometridae). By Mary Ellen Dix 


Outbreaks of the fall cankerworm, a hardwood defoliator in the Appalachian Mountain region of 
Virginia and North Carolina, were frequent between 1960 and 1973, but varied in duration and 
severity (Fedde et al. 1973). The cankerworm overwinters as eggs in masses attached to branches. 
Gerhard F. Fedde (SE, Research Triangle Park, NC) surveyed egg masses in Virginia and North 
Carolina for parasites. He found that Telenomus alsophilae was the most common of the three 
parasite species reared from the eggs (Fedde 1977; Fedde et al. 1973). This parasite was found 
initially in Connecticut in 1945 (Schread 1945) and later was collected in Virginia (Rauschenberger 
and Talerico 1967). Fedde also found that a very aggressive strain of 7. alsophilia attacked 
cankerworm eggs in the mountains of Virginia in late winter (Fedde et al. 1973). He described 
characteristics of parasite emergence holes that can be used to differentiate among the three parasite 
species (Fedde 1979). 


Telenomus alsophilae was a possible candidate for mass production and release because of its wide 
geographic distribution and high survival in fall cankerworm eggs. However, mass production 
required readily available host eggs that were easy to maintain. Fall cankerworm eggs are difficult to 
maintain in the laboratory, which made them poor candidates for rearing parasites. Fedde evaluated 
host preferences of T. alsophilae in the laboratory and found that the species could parasitize eggs of 
12 different species of geometrids and two species of noctuids. He concluded that the broad host 
range of this parasite made it the best candidate for mass rearing and release against lepidopterous 
eggs (Fedde 1977). 


Drooz, G.F. Fedde (SE, Research Triangle Park, NC) and Vicki H. Fedde (SE, Athens, GA) 
developed a technique for chilling host eggs so that they could be preserved in a state suitable for 
sustaining egg parasites (Fedde et al. 1979). They used this technique to maintain and mass-produce 
T. alsophilae on a surrogate host, the geometrid Eutrapela clemataria. Then the parasite was mass- 
released to control two geometrid defoliators in Colombia, South America. However, a laboratory 
test of the parasite against one of the pests, Glena bisulca on Cupressus lusitanica, was unsuccessful 
(Drooz and Bustilla 1972). In 1976, T: alsophilae was successfully established on the other 
geometrid, Oxydia trychiata, a native Colombian defoliator of introduced conifers and several 
species of hardwoods. Telenomus alsophilae was the first insect parasite to control a forest pest from 
a genus different from that of its natural host (Drooz et al. 1977b). 


4, Arthropod parasites and predators of the gypsy moth, Lymantria dispar (L.) (Lepidoptera: 
Lymantriidae). By Thomas M. ODell 


Introduction. The gypsy moth was introduced into Massachusetts from France in 1868. When initial 
attempts at eradication were abandoned, interest increased in the importation of exotic species of 
natural enemies to suppress populations of the gypsy moth and slow the spread of the pest. In 1904, 
the State of Massachusetts and the USDA Bureau of Entomology appropriated funds to import 
natural enemies of gypsy moth. In 1934, the Bureau merged with the Bureau of Plant Quarantine to 
become the Bureau of Entomology and Plant Quarantine (BEPQ). Abolished in 1953, this Bureau's 
forest pest research functions were distributed to the Divisions of Forest Insect Research and Blister 
Rust Control of the Forest Service (Dunlap 1980). Philip B. Dowden and Paul A. Godwin, both with 
some gypsy moth research experience in the BEPQ, were assigned to the Northeastern Forest 
Experiment Station's (NEFES) Forest Insect and Disease Laboratory, New Haven, CT. While in the 
BEPQ, Dowden conducted some of the earliest significant investigations on the biologies of gypsy 
moth parasites (Dowden 1933, 1934a and b, 1935). Dowden continued to work on the biology of 
gypsy moth parasites (Dowden 1961) at the NEFES Laboratory at New Haven, and conducted one of 


416 





the first, if not the first, inundative releases of Cotesia melanoscelus' (as Apanteles). The releases 
were made in the southern Lake Champlain region of Vermont, and resulted in no significant 
difference in percent parasitism by C. melanoscelus between treatment and control (Dowden and 
Reardon 1967). 


The foreign exploration and importation program for exotic parasites of gypsy moth, initiated by the 
Bureau of Entomology in 1904, has been one of the most massive efforts in biological control 
history. The Bureau's role in this effort is well documented by Reardon (1981a). This review will 
concentrate on the Forest Service's contributions to biological control of gypsy moth by arthropod 
parasites and predators between 1960 and 1990. 


Foreign Projects - Public Law 480. In the late 1950s, following extensive aerial application of DDT 
to eradicate gypsy moth infestations, the use of this pesticide was abandoned because of increasing 
concern about the effects of chlorinated hydrocarbons in the environment. The need for safer 
methods for controlling gypsy moth stimulated support for development of biological control 
techniques. In the early 1960s, efforts resumed to search for new natural enemies. Between 1960 and 
1975, the Forest Service, under Public Law 480, supported five overseas projects on the gypsy moth 
and its natural enemies, during which many natural enemies were imported into the U:S.: 

- Project in Spain, 1960-65: Project No. E25-FS-10 -- "The study of parasites, predators, and 
diseases of the gypsy moth and the possibility of their application in the biological control", 
conducted from May 11, 1960, to May 11, 1965. N. Romanyk, Servicio de Plagas Forestales, C. 
Marques de Mondejar 33, Madrid, Spain, was Principal Investigator. 

- Projects in India, 1961-71: Project No. A7-FS-8 -- "Survey for natural enemies of the gypsy 
moth", conducted from July 25, 1961, to July 24, 1966. V.P. Rao of the Indian Station, 
Commonwealth Institute of Biological Control, Bangalore-6, India, was the Principal 
Investigator. Project No. A7-FS-51 -- "Evaluation of hymenopterous parasites of gypsy moth and 
the study of the behavior of promising species" replaced the previous Indian project and was 
conducted from March 1, 1967, to August 31, 1972. V.P. Rao and P.R. Dharmadhikari, Indian 
Station, Commonwealth Institute of Biological Control, were the Principal Investigators. 

- Projects in Yugoslavia, 1967-77: Project No. E30-FS-9 -- "A biological method of control of 
injurious insects Lymantria dispar L. and Diprion pini L." was conducted from February 1, 1967, 
to December 31, 1971. Dr. Konstantin Vasic, Institute of Forestry and Wood Industry of Serbia, 
Kneza Viseslava 3, Belgrade, Yugoslavia, was the Principal Investigator. Project No. E30-FS-79 
-- "The effectiveness of certain parasites and predators to control gypsy moth" was conducted 
from April 1, 1972, to March 31, 1975. Dr. K. Vasic of the Institute of Forestry and Wood 
Industry of Serbia, was the Principal Investigator. This investigation was continued under Project 
No. E30-FS-79-JB-47, "Investigation of the possibility to use a pure line of gypsy moth with 
shortened diapause and Apanteles spp. for biological control of gypsy moth", December 22, 
1975, to November 30, 1977, again with K. Vasic as Principal Investigator. 


Summaries of these projects were prepared by Reardon (1981b). 


The "Accelerated" Research Program. In 1958, Robert W. Campbell (NEFES, New Haven, CT) 
initiated studies to investigate the population dynamics of gypsy moth. His life table analysis of 





‘Editor's (JRC) Note: When the species Apanteles melanoscelus was placed in the genus Cotesia by 
Mason (W.R.M.) (1981), there was some confusion among biological control authors as to the proper 
gender ending for the specific epithet, and the species is given as Cotesia melanoscela in some 
subsequent publications. However, according to R.W. Carlson, ARS Systematic Entomology 
Laboratory, Beltsville, MD (personal communication), Cotesia melanoscelus is grammatically 
correct, as is also indicated in Mason's paper. 


417 


outbreak populations in Glenville, NY, 1958-64, and sparse populations in Eastford, CT, 1965-68, 
suggested that arthropod parasites and a carabid predator, Calosoma sycophanta, had a minor role in 
gypsy moth population dynamics (Campbell 1981). These studies resulted in several publications 
which discuss, in part, parasite interaction in gypsy moth populations and their influence on gypsy 
moth behavioral evolution (Campbell 1963a and b, 1981; Campbell and Sloan 1976). 


In 1971, following a dramatic increase in gypsy moth defoliation through northeastern U.S., a 5-year 
accelerated research and development program was initiated. Along with "redirected" USDA 
research funds for university and state agencies, ARS and the Forest Service increased base funding 
and resources for gypsy moth research and development (McManus and McIntyre 1981). 


In 1972, as part of the Forest Service's accelerated research program, the Intensive Plot System (IPS) 
was established (Campbell and Bean 1971). The IPS, developed to expand on Campbell's earlier 
population dynamics studies, was comprised of six study areas of 12 hectares (29.65 acres) each in 
three states: two each in Massachusetts, New York, and New Jersey. Reardon (1981c) summarized 
the results of IPS parasite investigations in 1972 and 1973: 


"The 1972 and 1973 average percentage of parasitism data (12 and 14 percent, 
respectively) as determined by four collection techniques indicates that parasites by 
themselves, as an individual mortality factor, did not remove a significant proportion 
of the host population, and did not function to limit the rate of increase of the gypsy 
moth in these areas. Nevertheless, parasites did remove a portion of the host 
population and in combination with other mortality factors would have an influence 
on the rate of increase of the host." 


Specific parasite species relationships to site, gypsy moth, and disease have been documented by 
Reardon (1977) and Reardon and Podgwaite (1976). Unfortunately, investigation of the causes of 
gypsy moth mortality in the IPS was eliminated for economic reasons soon after it was initiated, thus 
limiting further development of information on the role of natural enemies in gypsy moth population 
dynamics. As Reardon (1981d) pointed out in suggesting areas for future parasite/gypsy moth 
research, there was still an "urgent need for the development and use of standardized techniques to 
sample host and parasite populations across many geographical areas," and a need for "intensive 
studies of those species established in North America as well as of exotic species" in order to 
"understand their specific ecological requirements and interactions with other species”. 


The Expanded Research Program. In 1975, the USDA responded to the need for additional methods 
to manage the increasing gypsy moth problem by planning and initiating the USDA Expanded Gypsy 
Moth Research and Application Program as part of the Combined Forest Pest Research and 
Development Program (Ketcham and Shea 1977). The Expanded Program complemented the 
accelerated effort and set specific objectives. The goals of the Program as set forth in Congressional 
hearings and the resultant appropriations bill included the statement that "The effectiveness of 
available and newly introduced parasites will be evaluated". The Expanded Program funded a 
number of extramural studies within the scope of this objective; however, only studies conducted 
directly or cooperatively by the Forest Service are summarized here. 


Between 1975 and 1980, an intensive laboratory and field evaluation of the tachinid Blepharipa 
pratensis was made (Godwin and ODell 1981). The general goal of the research was to determine, 
using population-study techniques, whether there was an aspect of the life history or behavior of this 
fly that would lend itself to manipulation so that the species could be managed as a biological control 
agent. Specific objectives were: 1) to develop methods to count the fly in its various life stages; 2) to 
identify major mortality factors required for the development of life tables and for the development 


418 











of population models; 3) to develop methods of rearing the fly in the laboratory; and 4) to describe 
the fly's reproductive behavior. 


Laboratory and field behavior investigations were carried out primarily at the USDA Forest Service's 
Forest Insect and Disease Laboratory Field Station, Branford, CT. Population studies were conducted 
in Eastford, CT, Washington Township, PA, and New Lisbon, NJ. The five-year investigation 
essentially accomplished its objectives: methods for sampling and assessing the viability of the 
various life stages were developed (ODell et al. 1974; Shields 1976; Godwin and ODell 1977, 1979, 
1981); mortality-causing agents were identified and a determination made of their impact on fly 
survival (Godwin and ODell 1981, 1984; Godwin and Shields 1984); components of the reproductive 
behavior of the tachinids B. pratensis and Parasetigena silvestris were identified (ODell and Godwin 
1979a, 1984; Godwin and ODell 1981); and a system for rearing B. pratensis in the laboratory was 
developed (ODell and Godwin 1979b; Godwin and ODell 1981). These results led to the formulation 
and implementation of an augmentative release of B. pratensis in 1978. Wild flies collected in 
Pennsylvania were held until egg laying was initiated. In June, 173 and 165 females were released in 
two 0.5-hectare study areas, respectively. Life stages of B. pratensis and gypsy moth were sampled. 
Based on host larval counts and parasite recovery in the two control sites, the host and parasite 
followed population trends expected in an areawide declining host population; however, in the 
release areas, instead of the expected 59% decline in B. pratensis observed in the control area, the B. 
pratensis population increased two-fold. This increase was attributed to the augmentative release 
(Godwin and ODell 1982). 


During the expanded program, preliminary studies were conducted to determine the feasibility of 
using parasites in combination with pathogens in an integrated approach for managing gypsy moth 
populations (Raimo and Reardon 1981). In 1975, Richard C. Reardon, Forest Service, Forest Pest 
Management, Hamden, CT, evaluated the inundative release of three parasite species, Glyptapanteles 
liparidis, C. melanoscelus, and Brachymeria intermedia, individually and in combination with 
Bacillus thuringiensis (Bt), against gypsy moth in forests in Centre and Union Counties of 
Pennsylvania. Treatment with parasites alone had no effect on defoliation or population levels as 
compared with controls. Bt provided significant foliage protection with or without parasites, 
indicating that the parasite releases had no effect (Reardon et al. 1976; Raimo and Reardon 1981). 


Raimo et al. (1977) conducted studies at NEFES, Hamden, CT, to show that C. melanoscelus could 
transmit the gypsy moth nuclear polyhedrosis virus (NPV) to gypsy moth larvae, and to develop 
methods of contaminating parasites that could augment efforts to initiate epizootics artificially in 
gypsy moth populations. These studies successfully demonstrated that C. melanoscelus is capable of 
transmitting lethal doses of NPV to gypsy moth larvae. In preliminary field investigations using 
parasites contaminated with virus, the combination of parasites and pathogens was shown to be a 
potentially feasible integrated pest management approach (Raimo and Reardon 1981). 


With support from the Expanded Gypsy Moth Research and Application Program, exotic parasites 
were again sought for establishment in northeastern U.S. Anastatus ?kashmirensis, an eupelmid 
parasite collected from the "Indian gypsy moth", and the braconid Aleiodes (as Rogas) lymantriae, a 
solitary larval endoparasite of gypsy moth in Japan, were sent to the ARS Beneficial Insects 
Research Laboratory quarantine facility in Newark, DE, in 1975 and 1978, respectively. 
Preintroduction evaluations were conducted for both species by William E. Wallner at NEFES, 
Hamden, CT. The evaluation of A. ?kashmirensis led to a recommendation that the parasite not be 
released, based primarily on the apparent ineffective role of A. ?kashmirensis as a primary gypsy 
moth parasite, its propensity as a facultative hyperparasite, and the difficulty of morphologically 
distinguishing A. ?kashmirensis from A. disparis, an egg parasite introduced earlier and known to be 
widely established in northeastern U.S. (Wallner 1981). 


419 


Evaluation of A. /ymantriae was conducted between 1978 and 1988. Laboratory experiments 
spanning 125 parasite generations included investigation of genetics, alternate hosts, host density 
factor effects on parasite sex ratio, and effect of Bt on parasitism rate (Wallner et al. 1982; Wallner 
and Grinberg 1984; Grinberg and Wallner 1991). Field releases of A. /ymantriae were made in eight 
states: New Haven area, CT, 1981, 1982, 1984; Cecil County, MD, 1982; Addison County, VT, 
1982; Provincetown, MA, 1983; Halley, PA, 1983; Loudoun County, VA, 1983; Gratiot County, MI, 
1983; Vermont (Sandgate, Colchester, Pownell, Milton), 1984; Maryland (Eastern Shore), 1985; and 
Corvallis, OR, 1986. Within-year recoveries of 4. /ymantriae cocoons were made in the majority of 
sites, but evidence of establishment has not been found (W.E. Wallner, personal communciation). 


Under a US/USSR Science and Technology Agreement, and arranged by the Working Group in 
Forestry, forest protection delegations representing the Forest Service, other USDA organizations, 
and cooperating state agencies, visited the Soviet Union to work with Soviet scientists in the field on 
integrated pest management of hardwood defoliating insects, including the gypsy moth. The first 
visit, in 1975, introduced the U.S. delegation to Soviet research on the gypsy moth and other 
hardwood defoliators, including research on population dynamics of gypsy moth (Simeone et al. 
1975). The second visit, in 1978, focused attention on biological methods of control of the gypsy 
moth and other forest pests (McKnight et al. 1978). The third visit, in 1981, focused on integrated 
pest management and provided an opportunity to import to the U.S. parasites that might be of use in 
limiting the severity of gypsy moth populations in the U.S. (McKnight et al. 1981). The visits 
provided an excellent opportunity to obtain information on the role of parasites of gypsy moth in the 
USSR that could be used in development of studies in the U.S. (see Simeone et al. 1975; McKnight 
et al. 1978, 1981). In addition, two species of parasites, C. melanoscelus and Compsilura concinnata, 
were shipped to the U.S. for evaluation and comparison with C. melanoscelus and C. concinnata 
populations present in northeastern U.S. The strain of C. concinnata from the USSR was being 
evaluated by P.A. Godwin, NEFES, Forest Insect and Disease Laboratory, but was lost in 1982, 
apparently to reproductive failure. The USSR strain of C. melanoscelus was evaluated by Mark 
Ticehurst at the Biological Control Laboratory, Pennsylvania Department of Environmental 
Conservation, Middletown, PA, for field release in 1982. 


In 1981, the USDA Office of International Cooperation and Development (OICD) sponsored the first 
U.S. forest protection team visit to the People's Republic of China (PRC). Led by Max W. 
McFadden, USDA Forest Service, the six-member team reviewed integrated pest management 
practices in the PRC and investigated opportunities for scientist and student exchange, and for the 
development of studies in integrated forest pest management research, including the exchange of 
biological materials (McFadden et al. 1982). As a result of this visit, a Scientific and Technological 
Cooperative Research Agreement on Natural Enemies of Gypsy Moth was developed. Under this 
agreement, six scientific team exchange visits were made between 1982 and 1988. Funding for the 
visits was borne, in part, by the OICD, the Forest Service, and the host institution in the PRC, the 
Chinese Academy of Forestry, under the Ministry of Forestry, Beijing. 


The objective of the first trip (1982) was to survey for natural enemies of the gypsy moth and 
evaluate them for potential importation into the U.S. for biological control purposes (Schaefer et al. 
1982). The three-member team, W.E. Wallner, NEFES, Hamden, CT, R.M. Weseloh, Connecticut 
Agricultural Experiment Station, New Haven, and P.W. Schaefer, ARS, Newark, DE, Team Leader, 
collected gypsy moth larvae in 11 different sites and confirmed the presence of 22 invertebrate 
parasite and 10 predator species. All of these natural enemies were considered for possible 
importation into the U.S., but official PRC policy prevented any living material from leaving the 
PRC at that time. Species diversity was greatest at Menjiagang, Heilongjiang Province, in northeast 


PRC, where gypsy moth population density was moderate. Population densities were low in the ten 
other collection sites (Schaefer et al. 1984). 


420 


In 1983, T.M. ODell, of Forest Service's Center for Biological Control of Northeastern Forest Insects 
and Diseases, Hamden, CT, and P.W. Schaefer, Team Leader, using the recommendations of the 
1982 team, returned to Menjiagang, Heilongjiang Province, to collect and evaluate the natural 
enemies of gypsy moth in this particular area. The team estimated that gypsy moth population density 
was 1/20th of that in the previous year. The cause of population decline from the previous 
"moderate" density in 1982 could not be determined. Egg masses were not easily found, but many old 
Glyptapanteles liparidis cocoons were found suggesting that this gregarious braconid may have 
contributed to the decline. In 1983, the US/PRC scientific team collected only 594 gypsy moth larvae 
in approximately 400 person-hours of intensive search; 71% of these were collected in three larch 
plantations under the bark of Larix spp. trees. Approximately 49% of the collected larvae produced 
parasites. Parasites emerged from 291 of the collected larvae; tachinids (Parasetigena and 
Blepharipa spp.) accounted for 70% of these; G. liparidis accounted for 30%. The relatively low 
population density of gypsy moth suggests that these parasites have excellent host searching 
capabilities. This year the U.S. team was allowed to export live insects to the U.S. Glyptapanteles 
liparidis cocoons, tachinid spp. puparia, and gypsy moth egg masses were received by the ARS 
quarantine laboratory, Newark, DE, in July 1983. This was the first importation of gypsy moth 
parasites from the PRC. Unfortunately, no adults emerged from the tachinid puparia, and the G. 
liparidis colony was lost due to poor mating and the subsequent absence of females (Schaefer and 
ODell 1983). 


In 1982, 1983, and 1986, delegations of Chinese scientists visited the U.S. to review biological 
control programs for forest insects and procedures for laboratory production of gypsy moth and its 
parasites. These trips resulted in the development of a proposal for a joint long-term study to 
determine the significance of the alternate host relationship of gypsy moth and "pine caterpillars" 
(Dendrolimus spp.) for maintaining parasite populations. 


In 1987, Andrew M. Liebhold (University of Massachusetts) and Carol B. ODell and T.M. ODell 
(Team Leader) (Center for Biological Control of Northeastern Forest Insects and Diseases, Hamden, 
CT) visited the PRC to help establish permanent research plots and initiate the "alternate host" study 
noted above. In addition, the team's objectives included assisting Chinese scientists to develop 
techniques for rearing parasites of "pine caterpillars" on gypsy moth, and selecting promising 
parasites for introduction and establishment in the U.S. 


The accomplishments of the 1987 US/PRC scientific exchange included: 1) a permanent plot was 
established in Yuan Ming Yuan Park, Beijing, for continuing research on natural enemies, 
particularly those which alternatively attack "pine caterpillars"; 2) two parasites, G. liparidis and 
Casinaria nigripes, were collected from "pine caterpillars" and successfully cultured on the gypsy 
moth; 3) G. liparidis was established on F, sterile gypsy moth larvae (via F,-sterile egg masses 
brought into PRC by the U.S. team), imported to the U.S., and successfully colonized for evaluation 
at the Forest Service's Insect Rearing Facility, Hamden, CT; and 4) the tachinids Exorista rossica and 
Exorista japonica were identified as the major parasites of gypsy moth emerging from large larval 
collections made in the Beijing plot. This was the first record of E. japonica on gypsy moth in the 
PRC; this species has been recorded as a parasite of Dendrolimus spp. (ODell et al. 1987). 


The US/PRC Scientific and Technological Cooperative Research Agreement on Gypsy Moth 
between 1982 and 1987 established an excellent scientific relationship and provided the biological 
basis for continuing cooperative investigations. Only five of the more than 20 parasite species 
recovered from gypsy moth collected in the PRC have been established in the U.S. from previous 
importation programs. One of the major reasons for this difference in parasite diversity is a lack of 
appropriate alternate hosts in the northeastern U.S. In the PRC, there are at least four and perhaps as 
many as 11 gypsy moth parasites that also attack "pine caterpillars" (ODell 1987). One of these, G. 
liparidis was recovered from gypsy moth at virtually all collection sites and at host densities ranging 


42] 


from sparse to moderate. The PRC G. liparidis strain, imported into the U.S. in 1987, and now in 
culture at the Forest Service's Insect Rearing Facility, Hamden, CT, is one of several parasites found 
in the PRC being evaluated for release in areas outside the northeastern U.S., where it has failed to 
establish after several releases (see Hoy 1976). 


Gypsy Moth Research and Development Program. In 1984, the Forest Service initiated a research 
program designed to develop the knowledge and technology that is necessary to maintain gypsy moth 
populations at economically and socially acceptable levels through integrated pest management 
techniques. Unlike some research programs before it, the Gypsy Moth Research and Development 
Program (GMRDP) for extramural research stressed maintenance of gypsy moth populations at low 
levels. Parasite research was included under two of the seven program objectives: "Develop the 
means to utilize parasites as regulators in low level gypsy moth populations", and "Evaluate the role 
of integrated pest management for gypsy moth". T.M. ODell, Center for Biological Control of 
Northeastern Forest Insects and Diseases, Hamden, CT, coordinated GMRDP parasite extramural 
research. The focus of the research was to obtain the information necessary to equate "percent 
parasitism" with generational mortality, i.e., evaluation of (real) parasite impact. The information 
developed includes the results of six years of field and laboratory experiments conducted by Joseph 
S. Elkinton, University of Massachusetts, and his graduate students. Information on competition 
between agents has been developed so that the capability of three parasite species (Parasetigena 
silvestris, Cotesia melanoscelus, and Brachymeria intermedia) to regulate gypsy moth populations 
was determined. In addition, information was developed for measuring the impact of parasites on 
generational mortality without specifically quantifying distribution and abundance of individual 
parasite species or guilds. The K factor analysis developed by Elkinton simplified all aspects of 
assessing the generational mortality due to parasites on host population dynamics, including host 
sampling in various stand types and host densities (Elkinton et al., 1989; Gould et al. 1989, 1990). 


Cooperative gypsy moth parasite research at the University of Maryland focused on developing 
methods for measuring parasite contribution to mortality usually recorded as "unknown." Under the 
direction of Michael J. Raupp, a method for measuring unknown mortality due to stinging by Cotesia 
melanoscelus was developed (Thorpe et al. 1990). The technique used in this study should be useful 
for similar studies with other parasites. 


Other gypsy moth parasite research conducted during the GMRDP included a survey of parasites in a 
mesic and adjacent intermediate and xeric forest habitat in Salisbury, VT (1984-85) directed by 
Bruce Parker, University of Vermont. The study was conducted when gypsy moth population density 
was <10 egg masses per acre. Results indicate that Compsilura concinnata was the dominant parasite 
in all three sites, for both years. Diversity and distribution during each year were determined 
(Skinner et al. 1993). Also, a laboratory study of the behavior of Ooencyrtus kuvanae, an egg parasite 
of gypsy moth, was conducted to discern the parasite's host selection response in different light 
regimes. The study showed that low levels of light significantly reduce host finding (ODell et al. 
1989). 


A major part of the GMRDP was the development of the Gypsy Moth Life System Model 
(GMLSM). The four main components of the GMLSM are: stand submodel, gypsy moth submodel, 
pathogen submodel, and predator/parasite submodel. The development of the predator/parasite 
submodel has resulted in the evaluation and summary of an extensive literature base. Six parasites 
(Ooencyrtus kuvanae, Cotesia melanoscelus, Blepharipa pratensis, Brachymeria intermedia, 
Parasetigena silvestris, and Compsilura concinnata) and one predator (Calosoma sp.) were 
simulated. Mortality caused by these natural enemies is affected by gypsy moth and natural enemy 
densities, and gypsy moth location. Development of this submodel is an on-going process. Further 
documentation and development of data on each species, and their compensatory interactions, are 
needed to ensure the submodel simulates the "real world" (Sheehan 1987). 


422 


The need to develop an integrated pest management (IPM) approach to the gypsy moth problem has 
been recognized as an important objective throughout the period of accelerated research and 
development (1975-present). The Maryland Gypsy Moth Integrated Pest Management Pilot Project 
(1983-87) was a cooperative effort of the Maryland Department of Agriculture and the USDA. 
Project funding and coordination was provided by the Forest Service, State and Private Forestry, 
Forest Pest Management (Reardon et al., 1987). Major emphasis was placed on evaluating the new 
technology developed from the GMRDP. This included the use of applied biological controls. 
Parasites were the only component of the natural enemy complex that was manipulated. Emphasis 
was placed on maximizing their diversity, abundance, and effectiveness through augmentation. This 
was accomplished by collecting and redistributing parasites from the generally infested areas that 
were not abundant in the project area (Reardon et al., 1987). In 1985, a Korean strain of Cotesia 
melanoscelus was released sequentially over a three week period at an average level of 12,000 
females per hectare in three isolated mixed-hardwood woodlots infested with gypsy moth in Queen 
Annes County of Maryland's Eastern Shore. The objectives of the study were to determine the effect 
of inundative releases of laboratory-reared C. melanoscelus on the mortality of the gypsy moth and to 
determine apparent rates of parasitism occurring in different gypsy moth habitats. The laboratory 
colony used to produce the released C. melanoscelus originated from the Kyeonggi Province of 
South Korea and was obtained from the ARS Beneficial Insects Research Laboratory, Newark, DE, 
during 1983. Significantly higher rates of parasitism were achieved, but the inundative release of C. 
melanoscelus failed to reduce gypsy moth populations, as determined from egg mass counts 
(Kolodny-Hirsch et al. 1988). 


Future Research. From 1992, forest insect research began an increased emphasis on understanding 
the ecological roles and effects of native and exotic insects, including established and exotic 
parasites of the gypsy moth. Two experimental techniques developed during the GMRDP will be 
increasingly important to research on gypsy moth biological control and its role in ecosystem 
management. In addition, in the fall of 1992, the USDA Forest Service Quarantine Laboratory, 
located in Ansonia, CT, was dedicated. This new research facility will have an important function in 
future gypsy moth biological control programs. 


One technique used by Forest Service scientists and cooperators since 1985 artificially manipulates 
host densities to study density-dependent relationships of gypsy moth. Using field-collected and 
laboratory-reared gypsy moth egg masses, high densities of trap hosts were created in otherwise low 
density gypsy moth populations. The results indicate that spatially density-dependent mortality 
caused by parasites is important in the maintenance of low densities (Liebhold and Elkinton 1989; 
Gould et al. 1990; Wilmot et al. 1994). In 1992, a study was initiated to document long-term changes 
in gypsy moth parasite species composition in ecologically diverse habitats along the "leading edge" 
of gypsy moth infestation in Virginia. This cooperative study, under the direction of Fred P. Hain, 
North Carolina State University, uses sterile gypsy moth larvae, derived from laboratory-produced 
F,-sterile egg masses (Mastro et al. 1989), to create small areas (1 hectare) of high host densities 
(Hasting et al. 1994). 


In 1991, the Forest Service began investigating techniques for identifying biotypes of biological 
control agents. Utilizing isozyme techniques, the genetic structure of populations of C. concinnata is 
being studied (Sanchez 1992). Correlation of breeding population genetics of C. concinnata with 
collection site (habitat) will enhance understanding of exotic parasite introductions and increase our 
capability for investigating the bioecology of gypsy moth parasites. 


The USDA Forest Service Quarantine Laboratory. The Forest Service Quarantine Laboratory at 
Ansonia, CT, is certified to confine and colonize entomophagous and phytophagous arthropods and 
entomopathogens for biological control research. The integrity of the 3100 square foot quarantine 
area is maintained by a double air lock entry/exit system equipped with light traps; three negative 


423 


pressure zones, each equipped with air conditioning, HEPA filtration and 100 mesh exhaust 
screening; double glazed, break-proof windows; a pass-through autoclave disposal system; and strict 
personnel protocols. An automatic generator maintains the negative pressure system during power 
failure and a professional security company monitors system failure, fire, and unauthorized entry. 
Environmental chambers provide space for rearing and studying large numbers of arthropods. All 
insect handling is performed inside HEPA-filtered biological safety cabinets to contain insects and 
protect worker health. Management of the facility is designed for cooperative research with state, 
federal, and international biological control projects. 


5. Development of "Gypchek™", a gypsy moth pathogen. By John D. Podgwaite and James M. 
Slavicek 


Development of the gypsy moth nuclear polyhedrosis virus (LdNPV) product, Gypchek™, can be 
traced to the early 1900s when Reiff (1911) speculated that the "Wilt disease" of gypsy moth 
caterpillars could be utilized to control the pest. Results of some limited field trials supported the 
concept (Glaser and Chapman 1913). At the time, however, spraying with lead arsenate was the 
popular gypsy moth control tactic and that tactic persisted, at least for large scale gypsy moth control, 
until the emergence of DDT in the 1940s. After a decade of environmental saturation with DDT, it 
became clear that this chemical was not going to eradicate the pest from North America and that it 
posed a serious health hazard to man and beneficial wildlife. The search for environmentally 
compatible pesticides then began in earnest, and interest in LNPV was renewed. 


Forest Service research on LdNPV began in the early 1950s at the Northeastern Forest Experiment 
Station's Laboratory on the Yale University campus in New Haven, CT. In a major reorganization 
that saw responsibility for forest insect research shift from the USDA Bureau of Entomology and 
Plant Quarantine to the FS, P.B. Dowden became the leader of a primordial Insect Pathology and 
Microbial Control work unit that would eventually grow to be the driving force behind the 
development and registration of Gypchek™. Dowden and F.B. Lewis, an entomologist within the 
unit, conducted some probing experiments to assess the effectiveness of LdNPV treatments 
(suspensions of field-collected NPV-killed gypsy moth larvae) on individual gypsy moth infested oak 
seedlings. Results from those experiments were encouraging and prompted the testing of LdNPV in 
combination with Bacillus thuringiensis (Bt) (which at the time was in its infancy as a microbial 
control agent) in a series of field trials in New York State in 1961-63 (Lewis and Connola 1966). 
Those field trials were undertaken more for the hope of increasing Bt mortality than for assessing the 
efficacy of LNPV. Results showed some LdNPV effectiveness but were compromised by what was 
later to be determined as antagonistic properties between Bt and LdNPV when the two agents were 
sprayed together. 


In 1963, F.B. Lewis, who had assumed the work unit leadership upon Dowden's transfer to ARS, and 
W.D. Rollinson tested NPV alone on a one acre (0.4 hectare) plot of mixed oak in the White 
Memorial Forest, Litchfield, CT (Rollinson et al. 1965). The treatment reduced the gypsy moth egg 
mass population in the plot by 95 percent but, more importantly, the results were instrumental in 
securing a strong FS policy and funding commitment toward developing gypsy moth NPV as a 
microbial insecticide. 


In 1965, two years after a fire had displaced the laboratory staff to temporary quarters in West 
Haven, CT, J.D. Podgwaite and H.M. Mazzone, both microbiologists, joined the work unit. Their 
studies focused on safety and production aspects of LdNPV and were in response to U.S. 
Environmental Protection Agency (EPA) directives that required candidate microbial pesticides to 
undergo a rigorous registration process, much the same as that required for chemical pesticides. At 
the time, the EPA directives were in the absence of firm guidelines and it was left to the scientists in 
the work unit to develop protocols and conduct tests with minimal input from EPA. From the results 


424 


of a variety of studies that followed (Lautenschlager and Podgwaite 1977, 1979; Lautenschlager et al. 
1978, 1979; Mazzone et al. 1976; Podgwaite et al. 1979), it became clear that although LdNPV was 
safe for man and the environment, it was not one of the more virulent insect viruses, and, further, it 
retained its pesticidal activity for only a few days following application to foliage (Lewis 1981; 
Lewis and Yendol 1981). 


In 1968, the work unit moved into permanent quarters in the Forest Insect and Disease Laboratory 
(now the Center for Biological Control of Northeastern Forest Insects and Diseases) in Hamden, CT, 
and work continued toward finding a more virulent LdNPV strain (than the original Connecticut 
strain), developing a cost-effective LdNPV-production system in collaboration with ARS scientists 
(Shapiro et al. 1981) and finally, developing a tank mix with sunlight protective properties. By 1972, 
progress warranted further field testing and, between 1973 and 1978, a variety of field experiments 
were conducted to evaluate several LdNPV formulations, dose rates, and spray systems against a 
range of gypsy moth populations (Yendol et al. 1977; Wollam et al. 1978; Lewis et al. 1979). From 
these evaluations emerged a direct aerial suppression tactic with LdNPV that under optimal 
conditions could be expected to provide 50-80% population reduction and enough foliage protection 
to prevent defoliation and subsequent physiological tree stress. 


In 1978, more than half a century after Reiff's insightful suggestions, Gypchek™, a technical product 
consisting of LdNPV-killed gypsy moth larvae that were dehaired, lyophilized and ground into a fine 
powder, was registered (EPA registration No. 27586-2) as a microbial pesticide. 


Unfortunately, the registration of Gypchek™ did not result in immediate widespread acceptance. The 
product was costly to produce and, compared to Bt products and other chemical pesticides, difficult 
to mix in a tank. Also, the product often clogged nozzle systems. Further, commercial producers were 
interested in developing products that would satisfy a broad market and were hesitant to commit 
substantive resources to a product that could be used against only one insect. So it was not surprising 
that in the early 1980s, with the growing acceptance of Bt as the microbial of choice for gypsy moth 
control and the emergence of the insect growth regulator (IGR) Dimilin™ in the market place, 
Gypchek™ was relegated to "specialty product" status. 


Research did continue toward developing an easy-to-use formulation containing an effective 
sunscreen. However, by the mid 1980s progress was minimal, and it became clear that Gypchek™ 
was becoming more of a "scientific curiosity" than an effective gypsy moth control agent. Then a 
series of changes occurred that once again brought Gypchek™ to the forefront. First, the technical 
product itself was modified from a "whole cadaver" preparation to a freeze-dried powder prepared 
from an aqueous blend of larval cadavers. That resulted in a more homogeneous product that did not 
clog nozzle systems. Second, the recommended dose was increased five-fold. Finally, an improved 
tank mix, incorporating the lignosulfonate sunscreen Orzan LS™, was developed. Field tests of the 
"modified" Gypchek™ and tank mix were very successful with results comparable to those obtained 
with Dimilin™ and Bt (Podgwaite et al. 1987; Podgwaite and Reardon 1989; Webb et al. 1989). 
Coincidental with these Gypchek™ successes, environmentalists were raising serious concerns as to 
the safety of Bt and Dimilin™ products for non-target insects and beneficial wildlife. Once again 
interest in Gypchek™ has rekindled, and the FS is working closely with industry partners in the 
development of a commercially-produced Gypchek™ that will be available for gypsy moth 
management in the near future. 


The Insect Pathology and Microbial Control Work Unit at Hamden, now headed by M.L. McManus, 
will continue to conduct Gypchek™ methods improvement research along several lines: the 
isolation, evaluation and field testing of naturally occurring LdNPV isolates that are more virulent 
than those found in the current product; the evaluation of genetically-modified LdNPV isolates 
having enhanced pesticidal properties; the development and field testing of "ready-to-use" 


425 


Gypchek™ formulations; and finally, the development and testing of a variety of Gypchek™ 
intervention tactics targeted to meet the needs of individual gypsy moth management programs. 


Gypchek™ research and development at Hamden has been truly a broad-based team effort and this 
brief historical accounting has only highlighted major events and developmental phases. In addition 
to those individuals cited above, the within-unit technical support of R.B. Bruen, P.D. Dusha, H.B. 
Hubbard, R.A. Lautenschlager, K.S. Shields, and R.T. Zerillo has been particularly valuable as has 
the long-standing support of FS-Forest Pest Management staff, in particular that of R.C. Reardon. 
The cooperative efforts of Animal and Plant Health Inspection Service (APHIS) and ARS personnel 
in the development of an LANPV production facility and the subsequent manufacture of a product by 
APHIS has been, and continues to be, vital as the FS transfers responsibility for Gypchek™ 
production to the private sector. Also, state and private organizations have played a major role in the 
effort; the Pesticide Research Laboratory at Pennsylvania State University, and the Boyce Thompson 
Institute for Plant Research at Cornell University are but two of many. Finally, all those that have 
lent support, but go unnamed here, are recognized for their contributions toward making LdNPV a 
safe and effective microbial pesticide. 


Biotechnology also offers a new approach for the development of improved biological and 
biorational control agents for forest insect pests and diseases. A new Research Work Unit, 
"Applications of Biotechnology in Forest Pest Management", located at the Forestry Sciences 
Laboratory, Delaware, OH, was created in the Northeastern Forest Experiment Station in 1987 to 
apply biotechnology to the area of biological control, and is now headed by Project Leader J.M. 
Slavicek. Scientists in the unit are focusing on development of Gypchek™ and other improved viral 
strains for use in gypsy moth control efforts that are competitive with other controls in terms of cost 
and efficacy. Enhancement of viral potency and efficacy (killing speed) would increase effectiveness 
of the Lymantria dispar MNPV (LdMNPYV). 


High viral production costs can be addressed indirectly through generation of a viral strain with a 
potency greater than that of Gypchek™. Efforts to enhance viral potency have focused on the 
identification of naturally-occurring isolates that exhibit biological activities greater than the 
Gypchek™ product. Several viral genotypic variants that exhibit potencies three-fold greater than 
Gypchek™ have been isolated (Slavicek and Podgwaite 1991). These isolates are being assessed as 
possible replacement viruses for Gypchek™. Other approaches for enhancement of viral potency 
may be devised once the molecular basis for viral potency is understood. Earlier studies have focused 
on the molecular characterization of the LdMNPV (Slavicek 1991a and b; Bischoff and Slavicek 
1993). Current efforts are focused on the identification of potency determinants in two LAMNPV 
genotypic variants that exhibit approximately 50-fold differences in potency. 


To mitigate the low viral efficacy, a genetically-engineered LAMNPV strain was generated that 
exhibits enhanced killing speed. To enhance viral killing speed the ecdysteroid UDP-glucosyl 
transferase gene was inactivated (Riegel and Slavicek 1993). This viral gene product prevents larval 
molting in virally infected insects. Insects infected with the engineered EGT-virus attempt to molt 
and in the process usually die. The overall effect is for infected insects to die earlier and, as a result, 
less foliage is consumed. 


Production of LdMNPV in cell culture bioreactor systems offers another approach to decreasing 
production costs (Slavicek 1992). Cell culture production systems offer the advantages of a cleaner 
product, ease of manipulation, and scale-up in comparison to production in gypsy moth larvae. 
However, an impediment to cell culture production is the high frequency of few polyhedra (FP) 
mutant formation during viral replication in cell culture. This viral mutant produces very few 
polyhedra, and those that are produced are essentially noninfectious (Slavicek et al. 1992). To solve 
this problem, scientists at Delaware have developed a LdMNPV viral strain that exhibits enhanced 


426 


polyhedra production stability during propagation in cell culture (Slavicek 1991c). A patent has been 
obtained for this viral strain (Patent # 5,420,031), and a Notice of Allowance was received from the 
U.S. Patent and Trademark Office on a patent application that covers the use of the improved viral 
strain for gypsy moth control. 


Further enhancement of viral potency and efficacy may be devised by manipulation of the processes 
of polyhedra formation and virion occlusion. Several LAMNPV mutants exhibiting abnormalities in 
these processes have been identified. Characterization of these mutants at the molecular level will 
identify viral genes involved in the processes of polyhedra formation and virion occlusion. 
Manipulation of these genes may generate viral strains with enhanced potency and efficacy traits. 


6. Spring cankerworm, Palaecrita vernata (Peck) (Lepidoptera: Geometridae). By Mary Ellen Dix 


The spring cankerworm severely defoliates Siberian elm, a tree commonly planted in field 
windbreaks in the northern Great Plains. In 1968, two branches of the Forest Service (Northern 
Region and the Rocky Mountain Forest and Range Experiment Station), and the University of North 
Dakota, conducted a successful demonstration of spring cankerworm control in field windbreaks with 
Bt. Formulations, application times, and application methods were compared for effectiveness in 
controlling spring cankerworm (Hard et al. 1979). A reevaluation of the sites in 1979 found that 
defoliation was reduced for more than one year (Hard 1979). 


Dix (Rocky Mountain Forest and Range Experiment Station, Lincoln, NE) observed a melyrid beetle, 
Malachius ulkei, feeding on spring cankerworm eggs. Late instar beetle larvae apparently migrate to 
Siberian elm windbreaks in early spring and feed on spring cankerworm eggs before crops germinate. 
She noted that M. ulkei disappears from the trees to move into crops about the time the cankerworm 
eggs hatch. Beetle larvae apparently search for food in the windbreaks when food is scarce in the 
surrounding crops (Dix 1991a). This was the first example of a benefical arthropod obtaining food 
and protection from tree windbreaks in a tree/crop ecosystem. 


7. Willow sawflies (Hymenoptera: Tenthredinidae). By Karen M. Clancy and Mary Ellen Dix 


The sawfly, Pontania sp. nr. pacifica, forms leaf galls on "arroyo willow" in northern Arizona 
(Clancy et al. 1986). In PhD dissertation research that was partially funded by the Forest Service, 
Karen M. Clancy (now with Rocky Mountain Forest and Range Experiment Station, Flagstaff, AZ) 
examined the importance of temporal variation in tri-trophic level interactions among the willow, this 
leaf-galling sawfly, and its natural enemies (inquilines and ectoparasites) from 1981 to 1984 (Clancy 
and Price 1986). The phenology of sawfly oviposition and larval development differed dramatically 
between two study sites at Flagstaff and Oak Creek, as did enemy-caused larval mortality. At Oak 
Creek, sawfly larval survival was high, mortality from natural enemies was low, and sawfly 
oviposition occurred early in the period of willow growth. In contrast, sawfly larval survival was low 
at Flagstaff, a high proportion of the larvae were killed by natural enemies, and oviposition occurred 
late in the period of willow growth. Offspring of sawflies that oviposited early at Flagstaff suffered 
higher rates of larval mortality from natural enemies than offspring of sawflies that oviposited later. 
Clancy and Price (1986) concluded that there may have been a phenological shift by the Flagstaff 
Pontania population to synchronize with "windows of time" that maximize survival and enemy-free 
space. Clancy and Price (1989) also determined that sawfly death from natural enemies was twice as 
much as from plant resistance and over six times greater than mortality from intraspecific 
competition. 


427 


8. Large aspen tortrix, Choristoneura conflictana (Walker) (Lepidoptera: Tortricidae). By Mary 
Ellen Dix 


In 1966, 1978, and 1983 the large aspen tortrix defoliated large areas of trembling aspen in interior 
and south-central Alaska (Beckwith 1968; USDA Forest Service 1983). Residential trees had reduced 
growth or were killed after several years of severe defoliation. The tortrix also periodically severely 
defoliates aspen in the coastal forests of Oregon, Washington, and British Columbia (Holsten and 
Hard 1985). 


Parasites and other natural controls are recognized as a factor in regulating tortrix populations. 
Typically, tortrix populations are high for several years before rapidly collapsing, apparently due to 
an increase in abundance of natural enemies. Torgersen and Beckwith (1974) identified 24 parasite 
species, described their biologies, and developed a key to the parasites. 


In 1980, commercial insecticides were unavailable to homeowners for control of the moth. Holsten 
and Hard (State and Private Forestry, Anchorage, AK) tested formulations of Bacillus thuringiensis 
(Bt) in the laboratory to determine their effectiveness in controlling the moth (Holsten and Hard 
1981). A 1981 field test to determine the efficacy of these liquid Bt formulations, was unsuccessful 
because the Bt was applied after the larvae had significantly defoliated the trees (Holsten and Hard 
1981). Holsten and Hard applied the Bt to younger larvae in 1983 and successfully controlled the 
tortrix and minimized defoliation (Holsten and Hard 1985). 


9. Bacillus thuringiensis. By Mary Ellen Dix, Leah S. Bauer and Al Valaitis 


The bacterium Bacillus thuringiensis (Bt) is an attractive alternative to chemical pesticides because it 
is non-toxic to the environment, relatively harmless to non-target organisms including beneficial 
parasites and predators, and selectively pathogenic against specific leaf-feeding insects. Because of 
the specificity of Bt, it can be used in combination with natural enemies and other control techniques. 


In the late 1950s, commercial preparations of the microbial insecticide Bacillus thuringiensis 
thuringiensis (Bt) became available for control of leaf-feeding Lepidoptera. Between 1960 and 1993, 
Forest Service and university scientists identified and screened Bt strains that could be used to 
control defoliators of hardwoods (gypsy moth [GM], cottonwood leaf beetle, and cankerworms) and 
conifers ("spruce budworms", Douglas-fir tussock moth, and hemlock defoliators). Studies also were 
conducted to understand the biology, mode of action and taxonomy, to improve potentcy of 
formulations and to develop and refine application techniques. Results of these cooperative efforts on 
GM have been summarized by R.C. Reardon, N.R. Dubois, and W. McLane in an unpublished Forest 
Service manuscript (Reardon et al. 1994). Although most research efforts on hardwood defoliators 
focused on GM as discussed here, results were applied to other defoliators and are discussed in those 
specific sections. 


Early research activities, 1961-69. During the 1960s, Forest Service entomologists designed studies 
to determine if Bt could be used to control leaf-feeding Lepidoptera, to screen Bt strains, and to 
obtain fundamental information needed to improve Bt effectiveness. In 1961, F.B. Lewis and D.P. 
Connola (Northeastern Forest Experiment Station [NE], New Haven, CT) initiated a three-year study 
to explore the possibilities of using Bt to control GM. Although their results were inconclusive, they 
determined that Bt could be effective in controlling the moth. They also improved formulations and 
application techniques, and gained considerable information and experience (Lewis and Connola 
1966). 


Lewis et al. (1964) evaluated various strains of Bt and found that they differed in potency. No 
relationships were found among taxonomically related Bt varieties and source insects. Cosenza and 


428 


Lewis (1966) biochemically characterized and determined the pathogenicity of four wild-type spore- 
forming Bacillus spp. that were isolated from dead or diseased GM. Using uniform growth 
conditions, N.R. Dubois (NE, New Haven) found that the activity spectrum of taxonomically-related 
Bt strains ranged greatly, and strains of different serotypes could have equal potency (Dubois 1968; 
Dubois and Squires 1971). But, larvae of similar age and different geographic populations differed in 
their susceptibility to specific Bt preparations. 


Although effectiveness of aerially-applied Bt was initially improved through strain selection, 
formulation modification, and improved foliage coverage, single aerial Bt applications were less 
effective than conventional insecticides. Lewis and Connola (1966) determined that multiple 
applications overcame the variation in larval developmental rates and susceptibility to Bt. They also 
showed that incorporation of compatible adjuvants improved the sticking quality of Bt on foliage. 
Dubois (1965) found that the addition of the sticker-antievaporant Pinolene #1674 to spore 
formulations extended spore viability and pesticide activity up to four times. Lewis and Connola 
(1966) observed that when a commercial preparation of Bt was diluted and then fed to GM larvae, 
feeding activity increased markedly, while feeding activity decreased when the GM were fed only 
washed crystal fractions. 


During early experiments, control of GM by aerial spraying Bt was evaluated solely on the basis of 
reduction in number of egg masses. This method did not allow separation of treatment effects from 
natural mortality. Connola et al. (1966) developed a method for correlating egg-mass density 
reduction with ten-minute larval counts in the field, frass collections, and defoliation counts. 


Accelerated research activities, 1970-79. Although fundamental studies during the 1960s provided 
information to develop Bt as an alternative pesticide, additional research was needed to develop and 
refine Bt application methods for practical and effective use. However, during the 1970s, most Forest 
Service research efforts on GM concentrated on nuclear polyhedrosis viruses (NPV) and efforts on 
Bt were minimal, except for participation in strain evaluation and comparison tests (Lewis and Etter 
1978). This extensive screening program was maintained because bioassays were the only reliable 
method to evaluate pesticidal activity of Bt strains. Most research on formulations, application 
methods, and impacts of Bt on GM parasites was conducted by non-FS scientists. An exception was 
an evaluation by Dubois et al. (1971) of mist blower ground applications in New Jersey and 
Massachusetts. 





In 1970, a new strain of Bt, HD-1, was isolated by ARS scientists and commercially produced that 
increased the pesticidal activity of Bt at least 15 times (Dulmage 1970). In 1972, Lewis et al. (1974) 
evaluated five formulations of Bt against GM in New York, New Jersey, and Pennsylvania. Although 
adequate coverage was obtained, rain reduced the effectiveness of these formulations. Subsequent 
tests by W.G. Yendol (Pennsylvania State University) and others determined that three different 
commercial preparations of a high potency Bt strain effectively reduced GM populations (Yendol et 
al. 1973). Foliage protection and larval mortality of these Bt preparations was not affected by 
application rate. Furthermore, foliage protection could last up to a month (Yendol et al. 1973). 
However, a subsequent study by Lewis et al. (1974) with aerially-applied Bt did not reduce GM 
populations to the desired levels, even though foliage protection was adequate. Rainy, cool weather 
was found to affect the results adversely. 


New strains of Bt were continually isolated. Dubois (1978) screened 350 isolates representing 14 
serotypes against GM larvae to determine the activity spectrum against GM. Dubois and Gunner 
(1974) found that numerous Bt strains from healthy GM larvae became pathogenic to their host after 
culture in chitinase-inducing media. Dubois (1977), in an extensive study on the pathogenicity of Bt 
to healthy GM, found that numerous chitinolytic microorganisms could be isolated from healthy 


429 


third-, fourth- and fifth-instar larvae. The acquisition of this microflora appeared to be associated 
with increased mobility of the maturing larvae. 


Research activities, 1980-93. Although considerable progress was made during the 1970s on the 
development of new strains, improved formulations, and multiple application techniques providing 
significant foliage protection, Bt performance was erratic in both ground and aerial tests. Extended 
GM egg hatch and development times, and short residual activity of Bt adversely affected results and 
reduced their acceptance. Also, the high cost of the product and the double application discouraged 
general and large scale use even in environmentally-sensitive areas (Dubois 1986). More potent 
strains, improved formulations with longer residual activity, and more effective application 
techniques were needed before Bt would be widely used (Dubois and Lewis 1981). 





By 1981, new strains and formulations were identified that exhibited potentially higher potency and 
longer residual activities than the standard HD-1 strain (Dulmage 1981). Dubois (1981) identified 
two laboratory strains (HD-243 and HD-263) of Bt with increased pathogenicity against GM. 
However, an aerial field test of these strains in Connecticut determined that they were less effective 
than the standard, commercially-available HD-1 strain, and that they, too, required two applications 
(Andreadis et al. 1982). Another strain (NRD-12), isolated in 1981 from spruce budworm, was found 
to have three to four times the toxicity of other strains against GM and other species of Lepidoptera. 
Field studies with this strain demonstrated less defoliation and longer effectiveness than the earlier 
test strains (Dubois 1985a and b; Dulmage et al. 1985; Dubois et al. 1988). Dubois (1986) also 
demonstrated that a synergism between Bt (HD-1) and a B-exotoxin increased susceptibility of GM 
larvae to Bt. However, strains and preparations that were most susceptible to GM were not 
necessarily the same ones that were toxic to spruce budworms (Dubois et al. 1989a). By 1990, Bt 
formulations had changed from oil-based to aqueous and contained adjutants (i.e., stickers) and 
ultraviolet screens that increased the persistence of Bt. 


In 1980, application costs were high because multiple applications of Bt were required to control 
GM. A cooperative trial by scientists of the University of Connecticut and the FS found that a single 
high-dose application gave adquate coverage, significant reduction in larval density and excellent 
foliage protection, if it was properly timed. This high Bt dosage was compatible with most natural 
enemies; parasitism by Cotesia melanoscelus increased, that by the tachinids Compsilura concinnata 
and Parastigena silvestris was unaffected, and that by Blepharipa pratensis decreased (Andreadis et 
al. 1983). Wallner et al. (1983) and Webb et al. (1989) also found that high doses of Bt did not 
adversely impact parasitism by the braconid wasps Aleiodes (as Rogas) lymantriae and C. 
melanoscelus. However, Weseloh et al. (1983), Wallner et al. (1989) and Woods et al. (1988) 
reported that levels of NPV decreased in GM after application of Bt, probably because larvae 
infected with NPV died prematurely. A cooperative study by the FS, APHIS, and Pennsylvania State 
University scientists demonstrated that high dosages of the Bt product Thuricide 64 LV™ was 
effective in reducing defoliation and egg mass density when applied to 3rd- and 4th-instar GM larvae 
(Dubois et al. 1991). This expanded the time available for Bt application. 


Coordination of research and application activities was improved by the establishment of a Bt 
technical committee in 1986 and a Forest Service National Steering Committee for Aerial 
Application of Pesticides Against Eastern Defoliators in 1988 also helped improve coordination of 
activities related to microbial pesticides. The establishment of the Northeast Forest Aerial 
Application Technology Group (NFAAT), an ad-hoc group of scientists and practitioners from the 
Forest Service, APHIS, ARS, Pennsylvania State University, and University of Connecticut, 
generated interest in the improvement of aerial application of Bt and other microbials. This group 
met several times a year to identify and prioritize research needs, and then jointly conducted 
laboratory and field studies designed to standardize methods and improve the performance of Bt 
(McManus 1990). Between 1989 and 1992, a series of studies was conducted to increase the efficacy 


430 


of Bt through improvement of ground and aerial application technologies. Dubois and McLane 
(1991) compared the effectiveness of hydraulic sprayers and mist blowers. 


Cooperative studies by scientists at Pennsylvania State University and Forest Service (M.L. 
McManus, NE, Hamden, CT) developed a technique that quantified the volume of spray deposition 
throughout the canopy at a single-leaf resolution (Yendol et al. 1990). Bryant and Yendol (1991) 
used this technique to determine the single-leaf deposition characteristics of aerially-applied Bt. They 
found that the quantity of spray arriving at the top and between each tree in the hardwood forest was 
highly variable. However, the average spray penetration was adequate to provide a lethal dosage in 
the lower canopy. Related studies (Dubois et al. 1989b, 1990, 1993) determined the most effective 
drop size and dispersal method at different volume rates and formulations. The optimal dose or 
volume of Bt varied with the GM outbreak stage. However, dispersal through the canopy and deposit 
on the leaves was most effective at rates of 7.0 liters/ha’. 


In 1988, a multi-year cooperative study among the Pesticide Research Laboratory at Pennsylvania 
State University, the Forest Meteorology Research Project at the University of Connecticut, APHIS, 
and Forest Pest Management's Appalachian Integrated Pest Management (AIPM) Project was 
initiated to evaluate, refine and adapt existing microbial insecticide technology for use in minimizing 
the spread of GM from the leading edge of the outbreak; the goal of the study was also to quantify 
the effects of local microclimate processes in and near the canopy on deposition patterns of aerially- 
applied Bt (Miller et al. 1990). Both Gypchek™ and Bt reduced numbers of egg masses and had 
similar levels of defoliation. However, only the control plots displayed a second wave of natural 
NPV mortality. Although these results were promising, additional studies are needed to determine 
how intervening with low-density microbials impacts GM population dynamics and to determine 
climatic conditions for optimal delivery of spray material (Podgwaite et al. 1993). 


High dosages of applied Bt, geographic variation in wild GM response to Bt, and the demonstrated 
resistance to Bt in some populations of other Lepidoptera species indicate the potential for 
development of genetic resistance of wild GM populations to Bt. Rossitor et al. (1990) studied 
resistance in three natural and one laboratory populations of GM by challenging 2nd-instar larvae 
with the HD-1 strain of Bt. Initial results of this study indicate that susceptibility variations are due to 
growth and development differences that are products of both the genotype and maternally- 
determined status of the egg. 


As a result of the identification of more potent strains and the development of improved application 
technologies during the 1980s by cooperative efforts among researchers, the use of Bt in operational 
control programs had changed from 2-4% of the total area treated for GM control in 1980 to over 
63% in 1990 (R.C. Reardon, unpublished data). The development of improved strains, delivery 
systems and insecticidal crystal protein technology will increase this percentage during the 1990s. 


Cry proteins. Studies during the past two decades have shown that the insecticidal crystal proteins 
(ICPs; i.e., 6-endotoxins, the Cry family of proteins) from the gram-positive Bt bacterium can be 
effective biological control agents for suppression of destructive insects in forestry and agriculture. 
Bt 5-endotoxins are protoxins which are converted by midgut proteinases in the target insect to form 
activated toxins with an apparent size of 60-65 kDa. The activated toxins bind to specific receptors 
on the surface of the midgut epithelial cells of susceptible insects, and cause rapid inhibition of 
potassium ion (K*)-dependent amino acid transport (Sacchi et al. 1986), changes in the permeability 
of the midgut membranes (Harvey and Wolfersberger 1979), and eventual lysis of the midgut 
epithelial cells and death of the insect. Ongoing research by FS scientists at Hamden, CT, and 
Delaware, OH (NE), and university cooperators is identifying Cry proteins toxic to GM and other 
forest defoliators, and determining their mode of action. 


43] 


Three insecticidal proteins produced by B. thuringiensis subsp. kurstaki HD-1 have been identified 
and designated as CryIA(a), CryIA(b) and CryIA(c). These three proteins differ in their primary 
structures, and these toxins exhibit significant variation in their insecticidal activity (Whiteley and 
Schnepf 1986; Dubois 1992). Although all three proteins are toxic to GM, only CrylA(a) shows any 
significant toxicity against silkworm larvae. Several factors, including synergism with microflora in 
the forest environment and solubilization of the ICPs and proteolytic activation of the protoxin, have 
been proposed to explain the differences in the insecticidal spectrum among the toxin proteins 
(Knowles and Ellar 1986; Haider et al. 1986; Dubois 1992; Dubois and Dean 1993). However, in 
many studies the main factor determining the specificity of a toxin in insects has been attributed to 
the presence or absence of a specific receptor in the midgut of susceptible and resistant insect larvae, 
respectively, and the degree of affinity of the receptor for the toxin protein (Hofmann et al. 1988; 
Van Rie et al. 1989, 1990a). 


The receptor for the CryIA(c) insecticidal protein in tobacco hornworm and GM was recently 
purified, and identified as the midgut brush border membrane-bound aminopeptidase-N (AP-N) by 
FS scientists in Delaware, OH (NE) and their cooperators. The purified receptors offer a means for 
rapid screening of 6-endotoxins from new Bt isolates that exhibit high affinity binding and activity 
with specific insect pests. The correlation of the presence of high affinity receptors and insecticidal 
activity indicate that binding is a crucial step in conferring toxicity. However, in some cases, the 
binding of Cry insecticidal proteins to the midgut membrane could not be corroborated with in vivo 
toxicity results (Wolfersberger 1990; Van Rie et al. 1990a and b). These results suggest that 
post-binding events, such as the ability of the toxin to integrate into the midgut epithelial membrane, 
contribute to the in vivo differences among the structurally related 6-endotoxins in their insecticidal 
properties. 


Studies of site-directed and homolog-scanning mutagenesis of the Bt 6-endotoxins have provided 
information concerning the functional domains and the location of specific regions of the 
6-endotoxins involved in receptor binding, and the irreversible interaction of the toxin with the insect 
midgut membrane (Schnepf et al. 1990; Ge et al. 1991; Wu and Aronson 1992). Similarly, future 
research that characterizes the molecular sites on the insect Bt receptors involved in binding these 
toxins, and the role of the receptors in facilitating the insertion of the toxin into the membrane will be 
valuable in elucidating the mode of action of Bt 6-endotoxins and should facilitate the rational design 
and synthesis of new, improved insecticidal proteins by protein engineering methodologies. Protein 
engineering may also be utilized to modify an existing Cry protein with respect to solubility, 
proteolytic stability, and receptor specificity and affinity. 


Because of the results of the many cooperative research efforts among federal and state scientists and 
applications personnel over the past 30 or more years, Bt has become the preferred method for 
control of GM and other forest defoliators. Future research will continue to advance the application 
technology and the understanding of Bt biology and its mode of action. 


D. Conifer Defoliators 


1. Blackheaded pine sawfly, Neodiprion excitans Rohwer (Hymenoptera: Diprionidae). By Mary 
Ellen Dix 


The blackheaded pine sawfly defoliates pines throughout most of the southeastern U.S. and Central 
America, causing serious damage to pine sawtimber in the Gulf Coast region (Thatcher 1971). In 
1966, W.H. Bennett (Pineville, LA [SO]) developed a problem analysis on natural control of sawflies 
affecting southern pine. Preliminary studies indicated that polyhedral viruses held potential for 
controlling these pests, but later inconclusive field studies, the lack of controlled temperature and 


432 


humidity units for rearing the insects to maturity and priority research on SPB in 1971 precluded 
more extensive studies on the blackheaded and other pine sawflies in Louisiana. 


A.T. Drooz, a Forest Service defoliator expert, and R.C. Wilkinson (University of Florida) identified 
larval and pupal parasites of the sawfly and two other Neodiprion spp. in northern and western 
Florida and Belize, Central America, and assessed their impacts on pines (Drooz et al. 1977a; 
Wilkinson and Drooz 1979). Because the parasites and fungal pathogens of sawflies in Belize and 
Florida were similar or closely related species (Wilkinson and Drooz 1979), no natural enemies were 
targeted for importation or later evaluation as potential biological controls. 


2. Parasites and predators of the Douglas-fir tussock moth, Orgyia pseudotsugata (McDunnough) 
(Lepidoptera: Lymantriidae). By Mary Ellen Dix 


The Douglas-fir tussock moth (DFTM) severely defoliates Douglas-fir and other true firs periodically 
in the Pacific Northwest and Canada. Outbreaks generally last two to four years before populations 
collapse in response to a combination of parasites, predators, diseases, and starvation (Mason and 
Wickman 1988). 


The importance of natural enemies in regulating DFTM populations has long been recognized. In the 
early 1930s, parasites were reared from DFTM eggs, larvae, and pupae (Balch 1932). During the 
1960s, nuclear polyhedrosis virus (NPV) and Bacillus thuringiensis (Bt) were used to control DFTM 
in a series of pilot projects conducted by entomologists of the Northern Region of State and Private 
Forestry (R-1, in Missoula, MT) (Tunnock 1966). Scott Tunnock identified causes of DFTM 
mortality at project sites in Montana and Idaho. He found that diseases (mainly a naturally occurring 
NPV) as well as parasites and predators contributed to the collapse of outbreaks after two to four 
years (Tunnock 1973, 1975). Boyd E. Wickman, Richard R. Mason, and Clarence G. Thompson of 
the FS Pacific Northwest Experiment Station (PNW) and other forest entomologists also observed 
similar collapses of outbreaks in Washington and Oregon and identified causes of the collapses 
(Mason and Thompson 1971; Tunnock 1973; Wickman et al. 1973). These scientists used parasite 
abundance to monitor the progress of DFTM outbreaks. Tunnock surveyed egg masses and predicted 
future defoliation levels in advance of several Forest Service pest management projects by comparing 
egg mass abundance with amount of parasitism and predation of the egg masses (Tunnock 1974; 
Tunnock et al. 1974). 


In 1974, research on DFTM parasites and predators and their impact on the population dynamics of 
DFTM accelerated after Congress approved the Expanded DFTM Research and Application 
Program. Robert D. Averill, Rocky Mountain Region, State and Private Forestry (R-2, Denver, CO), 
Scott Tunnock (R-1), Richard R. Mason (PNW), and Donald L. Dahlsten, University of California, 
Berkeley (UCB) studied DFTM outbreaks and non-outbreak populations in California, Oregon, and 
Washington. They reared and identified natural enemies of all DFTM life stages in Colorado, 
Montana, Idaho, Oregon, Washington, and California (Mason 1976, 1981a; Tunnock et al. 1976; 
Averill 1976; Dahlsten et al. 1977; Mason et al. 1983; Mason and Torgersen 1987). Torolf R. 
Torgersen (PNW) (1977) developed a key for identifying natural enemies of DFTM larvae. He 
described a new species of ichneumonid parasite, Hyposoter masoni, that was reared from first- and 
second-instar larvae collected at several sites (Torgersen 1985b). Torgersen and Mason (1979) also 
published a key to the parasites and predators of DFTM egg masses. Dahlsten et al. (1977) assessed 
the impact of NPV on natural enemy complexes in low to moderate DFTM populations. 


Egg parasites were found to play an important role in keeping population levels low. Rates of 
parasitism were evaluated in Colorado, California, and the Northwest (Mason 1976; Averill 1976; 
Dahlsten et al. 1977; Mason et al. 1983; Mason and Torgersen 1987). It was found in these studies 
that Telenomus californicus could parasitize more than 50% of the eggs, especially when DFTM 


433 


levels were low (Mason et al. 1983; Mason and Torgersen 1987), and that abundance of the parasite 
increased with decreased egg mass densities (Dahlsten et al. 1977). For these reasons, T. californicus 
was a good candidate for augmentative releases. In 1979, Torgersen and Mason began a series of 
one- to five-year studies to learn more about the parasite, including its range, geographical abundance 
over time, and the relationship between proportion of egg masses attacked and mean parasitization 
rate (Torgersen and Mason 1985). Successful parasitization of DFTM eggs by T. californicus was 
found to be dependent on parasite reproduction. Ryan et al. (1981) evaluated the effects of mating, 
female age, photoperiod, host storage temperatures, and host availability on reproduction of the egg 
parasite in the laboratory, and found that reproduction was greater in newly stored eggs than older 
eggs. Sower and Torgersen (1979) determined that applying a DFTM pheromone to a site did not 
interfere with host selection by the egg parasites. Thus, the pheromone and egg parasite could be 
used simultaneously to control DFTM. 


Although a number of natural controls had thus been identified, their role in the regulation of DFTM 
population at high and low levels was poorly understood. From 1976 to 1981, DFTM populations 
were periodically surveyed in California, Oregon, and Washington for natural enemies and the 
impacts of parasites and predators on DFTM abundance were assessed (Dahlsten et al. 1977; Mason 
et al. 1977, 1983; Torgersen et al. 1983; Mason and Torgersen 1987). Torgersen and Dahlsten (1979) 
found that arthropod and avian predators were major causes of larval mortality in non-outbreak 
populations of DFTM. They found that in most low-density populations, relatively few larvae were 
killed by parasites and disease compared to the number killed by predators. Stable DFTM 
populations apparently are rich in predaceous spiders, ants, birds, and other predators (Mason and 
Overton 1983; Mason et al. 1983; Mason and Torgersen 1987). 


Torgersen and associates used a stocking technique to assess predation on overwintering egg masses, 
larvae, and pupae in Oregon, Idaho, and California (Mason and Torgersen 1983; Torgersen et al. 
1983; Torgersen and Mason 1987). The most important predators of overwintering egg masses were 
birds (red-breasted nuthatch, dark-eyed junco, and Nashville warbler), and a tree-foraging ant 
(Camponotus sp.) (Torgersen and Mason 1987). Twenty-one species of birds were identified as 
predators or probable predators of DFTM larvae and pupae; nine species were observed feeding on 
larvae and pupae, and 12 species were observed foraging on tree branches from which larvae and 
pupae disappeared. The predominant larval and pupal predators were the red-breasted nuthatch, dark- 
eyed junco, and mountain chickadee (Torgersen et al. 1984b). The pentatomid Podisus serieventris 
was also an important larval predator. One P. serieventris was capable of destroying all stocked 
DFTM larvae in cages (Mason 1981b). 


During 1972-81, Mason, Dahlsten and colleagues identified and determined the distribution of 
spiders on Douglas-fir. They found that spiders were the most abundant predator in the system and 
that arthropod predation on early instar DFTM larvae was a key factor in DFTM survival (Mason 
1976, 1981b; Dahlsten et al. 1977; Mason and Overton 1983; Mason and Torgersen 1983; and Mason 
et al. 1983). Fichter and Stephen (1979, 1981) developed an ELISA (enzyme-linked immunosorbent 
assay) that permitted quantification of predation by polyphagous arthropods. Bioassays of spiders fed 
DFTM were positive for up to ten days after feeding. Similar assays of the pentatomid predator 
Podisus maculiventris were positive in half of the individuals for three days post feeding (Fichter and 
Stephen 1984). Scattered information on the identities and biologies of spiders was consolidated in a 


key to the most common arboreal spiders of Douglas-fir and true fir forests of the Pacific Northwest 
(Moldenke et al. 1987). 


The studies discussed above provided limited information on the relative densities and importance of 
spiders in regulating DFTM populations. In 1981, Mason began a study to compare the relative 
densities and importance of spider families on firs in the interior Pacific Northwest, Southern 
Cascades, Northern Cascades, and Blue Mountains (Mason 1992). Mason and Paul (1988) found that 


434 


Metaphidippus aeneolus, one of the most common arboreal spiders in the fir forest, readily preyed on 
small larvae in the laboratory and the field, and hypothesized that M. aeneolus was an important 
predator of the small larvae. Mason also found that spiders frequently outnumbered all other 
arthropod predators in the trees, and that species of each specific spider family inhabited a specific 
part of the foliage. Furthermore, familial structure and abundance of arboreal spider communities are 
similar within fir forests. Mason concluded that this underlying organization of spider communities 
should make spider populations more predictable (Mason 1992). 


3. Douglas-fir tussock moth pathogens. By Mauro E. Martignoni 


Outbreaks of the DFTM have occurred in many regions, from British Columbia to Arizona and New 
Mexico, from the Rocky Mountain states to the Cascade and Siskiyou ranges of Washington, Oregon, 
and California. Since the first reported infestation at Chase, BC, in 1916, several major outbreaks 
have occurred in stands where conditions changed rapidly in favor of tussock moth survival. Stoszek 
and Mika (1979) discussed the history of these outbreaks and described the site and stand 
characteristics associated with DFTM infestations. These infestations last typically about three years 
and usually terminate abruptly. Infectious agents were long suspected as a cause of epizootics among 
outbreak level populations of DFTM. A nuclear polyhedrosis virus (NPV) was first diagnosed in 
DFTM larvae collected in June 1947 by R.L. Furniss near Troy, OR (Steinhaus 1951). Larvae 
collected in August 1947 by J.C. Evenden in Colville, WA, and Orofino, ID, were also diagnosed as 
being infected with NPV. Both Furniss and Evenden considered the disease to be an important factor 
in the natural control of DFTM (Steinhaus 1951). Hughes and Addison (1970) found that two distinct 
NPVs, a unicapsid morphotype and a multicapsid morphotype, infected larvae of DFTM. Martignoni 
et al. (1969a and b) reported the occurrence of a cytoplasmic polyhedrosis virus (CPV) in DFTM. 


Research. In 1964, when DFTM outbreaks were in progress throughout the northwestern U.S., 
Clarence G. Thompson, head of the newly created insect pathology project ("Diseases of Western 
Forest Insects") of the Forest Service's Pacific Northwest Forest and Range Experiment Station 
(PNW), initiated a comprehensive program to develop a microbial control method using one of the 
NPVs of the DFTM (Thompson 1979). The insect pathology project was located in modern, well- 
equipped facilities at the Forestry Sciences Laboratory in Corvallis, OR. 


Initial laboratory studies in 1964 led to a small-scale simulated NPV field trial in 1965 (Thompson 
and Maksymiuk 1979). The positive results of this trial persuaded the Forest Service (FS), in 1966, to 
start a first Research and Development Effort ("Forest Service Joint Effort") to develop a viral 
insecticide against the DFTM. A pilot test by another branch of the FS in Idaho, in 1965, used a very 
low dose of NPV (10° polyhedral inclusion bodies per acre) and gave inconclusive results (Tunnock 
1966). Fortunately, this test did not have a negative impact on the decision to proceed with the 
development of a viral insecticide. The Forest Service Joint Effort included the following studies: 
virus characterization, acute toxicity-pathogenicity tests, pilot-plant scale virus propagation, 
production control procedures, formulation of spray mixtures, spray physics, and field tests. In 1973, 
all participants of the Joint Effort met to review the combined results and to prepare 
recommendations for future studies. In view of the promising results, the group decided to complete 
the toxicity-pathogenicity studies with the viral preparation and to apply to the Environmental 
Protection Agency (EPA) for an Experimental Use Permit (EUP) for the virus against the DFTM. 
The EUP was granted in 1974. Research on the virus was accelerated in 1974 through special 
one-year federal funding and greatly intensified in 1975 and following years under the new "USDA 
Expanded Douglas-fir Tussock Moth Research and Development Program". The appropriation bill 
for this program was included in the "Forest and Rangeland Renewable Resources Planning Act", 
signed into law by President Gerald Ford on August 17, 1974. Kenneth H. Wright, entomologist at 
the PNW station in Portland, OR, was appointed Program Manager of the large multidisciplinary 
research team. Research and application studies continued until 1978 along well defined activity 


435 


schedules, as outlined in Appendix 1 of the compendium on Douglas-fir tussock moth research and 
development (Brookes et al. 1978). This compendium was the culmination of many years of 
cooperative research by federal, state, and university scientists; it also served as a very effective 
avenue of transfer of knowledge on the DFTM to forest managers. 


During the period 1974-76, sufficient funding was provided to the PNW insect pathology project at 
Corvallis to complete additional laboratory and field studies. Virus strain identification, virus 
potency standardization, mammalian and fish toxicity-pathogenicity tests, and large-scale forest 
treatments with experimental virus preparations provided the knowledge needed to optimize virus 
dosage, timing, and spray strategies. These studies were urgently needed also because the EPA had 
reaffirmed its 1972 stand on the ban of DDT, then the only insecticide capable of effectively 
controlling DFTM. On February 26, 1974, the EPA granted the FS its last emergency authorization 
for the use of DDT against the DFTM in Idaho, Oregon, and Washington. Russell E. Train, then 
Administrator of the EPA, approved use of DDT against DFTM only "... with the greatest personal 
reluctance". In granting that application, Train also urged the FS to intensify research efforts and to 
find more environmentally-acceptable alternatives for controlling the moth (Train 1976). The 
intensive research and application work by the insect pathology project at the Forestry Sciences 
Laboratory at Corvallis provided ample data for final registration of the technical grade virus 
preparation. Registration of the product, named "BioControl-1™," was approved on August 11, 1976 
(EPA Registration No. 27586-1). Data on production, activity, and safety of the virus were 
summarized by Martignoni (1978) and results of the field efficacy tests were presented by Stelzer 
and Neisess (1978). As shown by these authors, the viral preparation proved to be safe and presented 
no undue risks to humans and the environment when sprayed in Douglas-fir forests. The field 
efficacy tests proved that DFTM populations could be controlled at an aerial application dose of 1.1 
x 10° viral activity units per acre, or about 10'' polyhedral inclusion bodies (PIB) per acre. Larval 
population reductions from 90-97% were reported and no insect survival to the pupal stage was 
observed in several treated plots. Significantly, viral applications also gave excellent foliage 
protection. 


At the height of research activities under the leadership of C.G. Thompson, the microbial control 
team at the Forestry Sciences Laboratory consisted of three entomologists, one microbiologist, one 
chemist, one electron microscopist, two entomology technicians, two microbiology technicians, one 
physical science technician, and one equipment specialist. In May 1977, Secretary of Agriculture 
Robert Berglund presented the team with a Science and Education Superior Service Award for 
outstanding effort in developing the use of the NPV product for control of the DFTM. 


Virus Propagation. Viruses reproduce exclusively within living cells. Therefore, successful mass 
propagation of viruses is linked to successful mass production of susceptible host cells. Based on 
propagation technology, production cost, and capital investment, living DFTM larvae are currently 
(1993) the preferred substrate for production of the NPV used for control of this pest (Martignoni 
1979, 1984). 


The FS awarded contracts for virus propagation in DFTM larvae to a private laboratory in 1966, 
1972, and 1974. The total output of these contracts was 9861 acre (3990 hectare) doses. Most of this 
material was urgently needed for the initial field trials and for toxicity-pathogenicity tests in 
mammals, birds, and fish. After 1974, it proved very difficult to find private laboratories willing to 
undertake production of virus at an acceptable cost. In 1979, a major production contract was 
terminated by the contractor because of difficulties and high costs associated with raising large 
numbers of larvae. 


In November 1980, FS Region 6 established a Baculovirus Production Facility (a field unit of Forest 
Pest Management) at the Forestry Sciences Laboratory in Corvallis, OR. The facility was organized 


436 


into three work sections: insect diet production, insect production, and virus propagation. Further 
details of the work at the facility are provided by Bergstrom (1985). The first manager of the 
Baculovirus Production Facility, from 1980 to 1985, was Donald W. Scott. Since 1985, Anita S. 
Hutchins has been manager of the facility. Mauro E. Martignoni, of the Forestry Sciences 
Laboratory, was adviser to the facility until the end of 1985. Depending on required production 
levels, the number of laboratory technicians and aides at the facility varied from a low five to a 
maximum of 12. The output, measured in amount of virus required to treat one acre (2.471 hectares) 
of forest, varied from a low of 30,000 acre (74,130 hectare) doses per year to a maximum of 100,000 
acre (247,100 hectares) doses per year. The total product now (1993) stockpiled under refrigeration 
is sufficient to treat approximately 400,000 hectares (988,400 acres) (Anita S. Hutchins, personal 
communication). 


The Baculovirus Production Facility was closed in June 1993, except for a minimum of technical 
personnel and equipment dedicated to maintenance of DFTM strain GL-1, the inbred strain used for 
bioassay of virus production lots. 


The virus propagated at the facility was exclusively strain MEM-75-STANDARD of the multicapsid 
NPV (Baculovirus, OpPMNPV) of DFTM. Since 1978, the passage level of this virus strain was 
stabilized by adoption of a seed-lot system (M.E. Martignoni, unpublished data). A large primary 
virus lot ("seed lot") was prepared and preserved in numbered ampoules under refrigeration. Each 
ampoule serves as inoculum for propagation in a small batch of larvae (first passage). Virus 
harvested from these larvae ("secondary inoculum") is used for inoculating production larvae (second 
passage). Thus, no more than two passages separate the final product from the 1978 seed lot virus. 
There is still (1993) a substantial supply of the original seed lot for future use. Virus strain 
MEM-75-STANDARD is also preserved as ATCC VR-992 at the American Type Culture Collection, 
Rockville, MD. 


Although the Baculovirus Production Facility was capable of producing and testing NPV, the 
material had to be processed in a way that guaranteed concentration of viral inclusion bodies and 
exclusion of unwanted larval debris. Packaging must assure long-term stability of the agent. Virus 
processing is achieved by wet slurrying of larval cadavers, centrifugation of the slurry, lyophilization 
of the clean sediments, screening, and vacuum packing; these operations must be done with methods 
and equipment that permit a high rate of recovery of active virus. When the Facility was established 
in 1980, those involved in planning were aware that private industry would have the equipment and 
knowledge needed to accomplish this work, whereas the FS had the best knowledge and personnel 
for rearing tussock moth larvae and propagating the virus. Thus the FS facility was not furnished 
with the costly equipment needed for this processing phase. That decision proved correct. The major 
processing contractor for BioControl-1™ was Espro, Inc., of Columbia, MD. The first of several 
contracts awarded to Espro by the FS was signed in June 1988 (Aldis E. Adamson, personal 
communication). About 90% of the virus produced by the facility had been processed by 1992, when 
the last contract expired and Espro was acquired (in a joint venture) by Crop Genetics International 
and DuPont. 


The cost of production of BioControl-1™ is determined principally by the cost of rearing the DFTM. 
The rearing cost can account for up to two-thirds of the total production cost. The latest (January 
1991) estimate of the cost of BioControl-1™ was just under $8 per acre-dose, processing and 
packaging included (A.S. Hutchins, personal communication). This cost is certainly acceptable in the 
context of long-term management of valuable Douglas-fir stands. 


Concluding Remarks. Research accomplished during 15 years (1964-78) by the insect pathology 


team at the Forestry Sciences Laboratory in Corvallis, OR, demonstrated that a Baculovirus is an 
effective and host specific control agent for DFTM larvae. It is an environmentally safe agent and an 


437 


economically feasible alternative to chemical insecticides. BioControl-1™ is the first virus registered 
in the U.S. for use against a forest insect. The viral product and the forest application strategies 
developed by the FS team have been integrated into practical forest management systems. A 
substantial amount of virus is stockpiled by the FS for use against future DFTM outbreaks. The goals 
of the Expanded Douglas-fir Tussock Moth Research and Development Program and the mandates of 
the EPA concerning microbial control of outbreaks of this forest insect were fully met. 


4. European pine sawfly, Neodiprion sertifer (Geoffroy) (Hymenoptera: Diprionidae). By Mary 
Ellen Dix 


The European pine sawfly, an introduced species, was first recorded at Somerville, NJ, in 1925 
(Schaffner 1939). It defoliates red and other pines from New England and southwestern Ontario, 
west to South Dakota and south to Missouri. In 1977, the ichneumonid parasite Lophyroplectus 
oblongopunctatus was successfully introduced to control this sawfly (Kraemer et al. 1979). In 1980, 
M.A. Mohamed and associates collected parasitized sawfly cocoons from Wisconsin field sites and 
overwintered them in the laboratory. The next spring they sprayed an aqueous suspension of a 
nuclear polyhedrosis virus from the European pine sawfly on the emerging L. oblongopunctatus. The 
infected parasites successfully transferred the virus to the sawfly larval colonies in the field 
(Mohamed et al. 1981). 


5. Hemlock defoliators. By Mary Ellen Dix 


Outbreaks of the hemlock sawfly, "blackheaded budworm", and the western hemlock looper severely 
defoliate western hemlock in Washington, Oregon, southeast Alaska and northwestern Canada. 
Heavy tree mortality followed severe sawfly and budworm defoliation during the early 1950s and 
1960s (Downing 1957; Crosby 1965) and a severe looper outbreak in Alaska during the mid-1960s 
(Torgersen 1971). 


Natural enemies can play an important role in regulating populations of both the sawfly and the 
looper. Torgersen (1968) identified parasites reared from hemlock sawfly cocoons, noted their 
abundance, and developed a key to the larval remains of seven parasites of the sawfly (Torgersen 
1969). This key can be used to assess levels of sawfly parasitism and predict control needs. 
Torgersen also reared eight species of parasites from pupae of the hemlock looper and developed a 
key to the ichneumonid parasites (Torgersen 1971). 


A 1963 field test of Bacillus thuringiensis (Bt) against the looper in southwest Washington was 
unsuccessful because lethal doses of Bt did not persist in the crowns (Carolin and Thompson 1967). 


6. Introduced pine sawfly, Diprion similis (Hartig) (Hymenoptera: Diprionidae). By John H. Ghent 


The introduced pine sawfly, a pest native to Europe and Siberia, was discovered in Connecticut in 
1914 (Britton 1915). In 1977, the sawfly was collected for the first time in North Carolina, in the 
Linville Falls area of Avery County. A survey of the introduced pine sawfly population in North 
Carolina during the winter of 1978 revealed that less than one percent of the sawfly larvae were 
parasitized (Drooz et al. 1979). The sawfly population was expected to increase and cause extensive 


damage to the area's white pine because of the lack of natural controls and the pest's bivoltine life 
cycle. 


In 1979, a research and applications program was initiated by Forest Pest Management and Forest 

Insect and Disease Research. J.H. Ghent (Forest Pest Management, Southeastern Region) and A.T. 
Drooz (Forest Insect and Disease Research, Southern Forest Experiment Station) were directed to 

develop and run a parasite rearing facility in the Linville Falls area (Drooz et al. 1985a). 


438 


They selected the torymid parasite Monodontomerus dentipes for rearing because it had reduced 
abundance of the introduced pine sawfly during an earlier outbreak in Wisconsin (Coppel et al. 1974; 
Drooz et al. 1985a). In 1979, introduced pine sawly cocoons were collected from populations near 
Amery, WI. Emergent parasites from this collection were used to initiate a mass-rearing program for 
M. dentipes (Fedde 1975). From July 1979 until the spring of 1981, a total of 14,000 parasites were 
released in North Carolina. Parasitism rose from 0.8% in 1979 to 44.9% by the winter of 1980. By 
the spring of 1981, introduced pine sawfly populations had effectively collapsed around the release 
area and the parasite rearing facility was closed (Drooz et al. 1985a). Over a decade later, M. 
dentipes still helps keep populations of the introduced pine sawfly below outbreak levels. 


7. Jack pine budworm, Choristoneura pinus Freeman (Lepidoptera: Tortricidae). By Mary Ellen 
Dix 


The jack pine budworm, a native species, severely defoliates jack pine in the Lake States. Outbreaks 
occur sporadically at six- to ten-year intervals and persist for two to four years (Benjamin 1956). 
Numerous university and Forest Service scientists have identified natural enemies and evaluated their 
impacts. In 1954, Benjamin and Drooz (1954) identified an egg parasite, six larval parasites, and ten 
pupal parasites in Michigan. They noted that two parasites, toplectis conquisitor and Apanteles 
fumiferanae, appeared to be important in reducing budworm populations. 


In 1965, entomologists at the University of Michigan initiated a study on the population dynamics of 
the jack pine budworm that included assessment of the impact of predators and parasites on budworm 
populations. They reared 26 species of parasites and four species of hyperparasites from the 
budworm. Parasitism was highest in second instar larvae. Apanteles (sens. lat.) sp. and Glypta 
fumiferanae were the most abundant parasites of the second-instar larvae, and 1. conquisitor was the 
most important pupal parasite (Allen et al. 1969). W.J. Mattson (North Central Forest Experiment 
Station) and cooperators found that 28 species of birds and mammals attacked budworms in 
Michigan. Bird predation helps regulate endemic budworm populations, but apparently was also an 
important mortality factor in large forests during budworm outbreaks. In small forests, bird predation 
was high because non-resident birds moved into the jack pine community and added to mortality 
caused by resident birds (Mattson et al. 1968). During the late 1960s, D.T. Jennings (North Central 
Forest Experiment Station) studied predators of the budworm in Minnesota and Wisconsin. He 
identified six species of ants in Wisconsin that actively preyed on late instar larvae of jack pine 
budworm after they were inadvertently dislodged from their feeding sites (Jennings 1971). The North 
Central Forest Experiment Station budworm project ceased because supporting funds were no longer 
available in the early 1970s, and Jennings transferred to New Mexico, in 1968. 


8. Larch casebearer, Coleophora laricella (Hiibner) (Lepidoptera: Coleophoridae). By Roger B. 
Ryan 


The larch casebearer was discovered on tamarack in Massachusetts in the late 1800s, presumably 
having arrived from its native Europe as an inadvertent introduction on planting stock. From there, its 
population spread and intensified throughout much of the northeastern U.S. and southeastern Canada 
and dispersed westward. 


Research on biological control of the larch casebearer in North America has passed through three 
rather distinct phases. Although serious defoliation of tamarack occurred in some areas for over 40 
years, the first phase of biological control research did not begin until the 1930s, when European 
parasites were released. Studies of the biology of larch casebearer and its natural enemies in Europe 
(e.g., Thorpe 1933; Eidmann 1965; Jagsch 1973) furnished valuable information to guide that and 
subsequent biological control efforts in North America. Between 1931 and 1939, the governments of 
Canada and the U.S. collected host material in central Europe and released several species of 


439 


parasites (Dowden 1934a and b, 1962; Dowden and Berry 1938; Graham 1944, 1949, 1958; Webb 
1953; McGugan and Coppel 1962b; Clausen 1978; see also Chapter II of this publication). Thorpe 
(1933) suggested that the ichneumonid Diadegma laricinellum (as Angitia nana) was the most 
promising biological control agent. P.B. Dowden, later of the Northeastern Forest Experiment Station 
and then working at the Bureau of Entomology Gypsy Moth Laboratory at Melrose Highlands, MA, 
initially reported (Dowden 1934a,) that only three species were "true internal parasites suitable for 
liberation". These were the species recommended by Thorpe, D. Jaricinellum, plus Agathis pumila 
(as Bassus pumilus) and Chrysocharis laricinellae. Dicladocerus westwoodii, an external parasite, 
was not initially released, probably because Dowden felt that "in general external feeders are 
polyphagous [and] sometimes develop on primary parasites" (Dowden 1941). Dowden initially 
released only the three internal parasite species named above, but in 1936, after investigating the 
biology of D. westwoodii, released it as well (Dowden 1962). Although Dowden also reported the 
release of two species of “"Horogenes", they were both later considered to be Diadegma laricinellum 
(Carlson 1979). The Canadians released the same four species and Cirrospilus pictus. Dowden, 
however, considered the hyperparasitic tendencies of C. pictus sufficient grounds to deny its release; 
he also reported that it was already in North America (Dowden 1941). 


Collections of larch casebearer in Europe were made at two different times in the spring, an early 
collection to obtain overwintering C. /aricinellae, and a later one when larvae were feeding, to obtain 
other parasite species. Diadegma laricinellum proved elusive to obtain from European collections. In 
Canada, a total of only 200 was released at three sites in four different years (McGugan and Coppel 
1962b). In the U.S., the numbers released were higher, 3580 adults at seven sites over five years, but 
Dowden (1934a) reported that the adult parasites emerging from European collections died before 
susceptible host larvae (needleminers) were present in U.S. field release sites. Releases probably 
were too small and ill-timed to give the species a reasonable chance for establishment of D. 
laricinellum. On the other hand, the release dates reported for D. westwoodii (McGugan and Coppel 
1962b) were probably too late for the adults to parasitize susceptible host larvae. Only two species, 
A. pumila and C. laricinellae, became established. 


In spite of the failure of two of the parasite species to establish, results of the biological control effort 
during that first phase were gratifying. The buildup of A. pumila coincided with decreased larch 
casebearer populations (Graham 1949), a pattern that was repeated as the pest dispersed westward. 
Chrysocharis laricinellae was slower to increase and in many areas increased far less than A. pumila. 
There were suggestions that C. /aricinellae might be a negative contributor to biological control 
because it parasitized hosts already containing A. pumila (Graham 1949). When most unparasitized 
hosts are in the pupal stage, C. laricinellae attacks a higher percentage of Agathis-parasitized than 
unparasitized larvae apparently because the prolonged development of the parasitized individuals 
makes them available for parasitization for a longer period; critical assessment of this interaction, 
however, was not addressed until later (Quednau 1970a). 


This first phase of biological control extended through the 1950s as the host dispersed westward into 
the Lake States on tamarack; established parasites were released in the new areas from previously 
established populations (Webb 1953, 1957; Coppel and Shenefelt 1960; Webb and Denton 1967; 
Webb and Quednau 1971). 


The second phase of biological control, confined to eastern North America, took place during the 
1960s and 1970s when biological research on the host and its natural enemies intensified (Cody 
1963; Sloan 1965; Sloan and Coppel 1965a, b, and c, 1968; Quednau, 1966, 1967a, b, and c, 1968, 
1969, 1970a and b; Cody et al. 1967; Coppel and Sloan 1971; Rush 1972; Raske and Schooley 1979). 


F.W. Quednau, stationed at the Canadian Department of Fisheries and Forestry's Forest Research 
Laboratory at Sainte-Foy, Quebec, conducted detailed investigations of the larch casebearer and its 


440 


parasites, including life-table work to assess the interaction between A. pumila and C. laricinellae, 
that highlighted this period (see above cited references). According to his assessment, the view that 
C. laricinellae detracted from biological control neglected to attribute on the plus side to C. 
laricinellae the additional fraction of the host population parasitized by its previous generation(s) but 
not by A. pumila (Quednau 1970a); C.laricinellae thus adds mortality to the casebearer generation 
that A. pumila cannot. Quednau concluded that, on balance, C. laricinellae contributed positively to 
biological control. Although A. pumila was clearly the dominant species in biological control in 
many areas, C. Jaricinellae was an important contributor and, in fact, seemed to dominate in certain 
situations, particularly in the Maritime Provinces of Canada. 


In addition to his life-table work in the field, Quednau (1967b and c, 1970b) added detailed 
biological knowledge on the casebearer and the two established parasites through laboratory rearings. 
He also renewed efforts to establish the particularly promising species, D. /aricinellum, that had not 
been established in the first phase (Otvos and Quednau 1984). His approach was to establish a 
laboratory culture for studying its interaction with A. pumila and which would serve as a source of 
inoculum for the eventual release of D. laricinellum (Webb and Quednau 1971). However, the 
parasite proved as elusive to collect as before and few were released. Inability to culture continuous 
generations of the host in the laboratory also indicated that a parasite that spends almost a year in the 
host larvae could likewise not be cultured. Quednau's research on the larch casebearer was 
terminated in 1974 by administrative reorganization and reallocation of effort within the Canadian 
government. 


The long-distance dispersal of the insect pest onto western larch in Idaho in the late 1950s (Denton 
1958) ushered in the third phase of larch casebearer biological control -- the parasite introduction 
effort in the West. The U.S. Forest Service's Intermountain Forest Research Experiment Station 
(INT) initiated research on the new pest in 1960. There were several studies of its biology, natural 
enemies, and effect on the larch resources of the West (Denton 1965, 1979; Andrews 1966; Andrews 
and Geistlinger 1969; Bousfield and Lood 1970, 1973; Denton and Tunnock 1972; Ciesla and 
Bousfield 1974; Ross 1976; Denton and Theroux 1979). 


The INT's then Chief of Forest Insect Research, D.E. Parker, cognizant of the successful biological 
control in the East, seized the research opportunity to see what A. pumila could do in the West 
without having to interact with C. /aricinellae (Anonymous 1960). Arrangements were made with 
Dowden, who collected parasitized casebearers from the Northeast, reared out A. pumila, and 
shipped adults to R.E. Denton, at the INT station in Missoula, MT, who made the first releases in 
northern Idaho in 1960 (Denton 1972). Other species were not released. Recoveries were made in 
1963 (Denton 1972). Forest Pest Management of the Northern Region headquartered in Missoula, 
MT, then became involved in further releases to spread more rapidly the establishing 4. pumila. 
Entomologists in State and Private Forestry in the Northeast made additional collections of 
parasitized larch casebearers in Massachusetts and Vermont and shipped them to northern Idaho for 
rearing of overwintering larvae to obtain adult A. pumila. The rearing effort over the next several 
years was the combined effort of INT and Forest Pest Management. Whole-tree cages were used to 
obtain parasitism of the Idaho larch casebearer population with parasites from the East (Denton 
1979). Between 1965 and 1969, parasitized overwintering casebearers were distributed by Forest 
Pest Management to approximately 400 sites in Idaho, Montana, and, with entomologists from 
Region 6 and British Columbia, to many sites in those areas as well, virtually blanketing the 
then-infested larch stands in the U.S. Subsequent evaluation revealed that A. pumila had become 
widely established (Bousfield et al. 1974). 


By about 1970, the expected collapse of the larch casebearer population failed to occur in the West 


and there was still widespread and severe defoliation, although green pockets of undefoliated trees 
were noted to surround some release sites. Nevertheless, widespread disappointment with the results 


44] 


of biological control led foresters to fear that larch, an important timber tree in the West (Schmidt et 
al. 1976), may be lost due to this pest in much the same way that white pine apparently was lost due 
to white pine blister rust. Some research on chemical control was going on at the time (Denton 1967; 
Denton and Tunnock 1968; Lyon and May 1970), but biological control research seemed to have 
stalled. Indications were that the larch casebearer would continue to be a serious problem (Tunnock 
et al. 1969). Indeed, larch was temporarily omitted from management plans. 


INT Assistant Director C.A. Wellner convened a strategy meeting in January 1971. It was decided 
that an all-out Research and Development (R&D) effort was called for. INT spearheaded a proposal 
to the Forest Service Washington Office to back and obtain funding for a "big bug" program on larch 
casebearer. The proposal called for expanded research on biological and chemical control and almost 
every other conceivable research area. In the next several years there was a flurry of effort in many 
areas, both inside and outside the Forest Service (Amman and Tunnock 1971; Tunnock et al. 1972; 
Ciesla and Bousfield 1974; Miller and Finlayson 1974, 1977a and b; Ryan 1974a and b; Hansen 
1977, 1980, 1981; Long 1977; Moody 1977; Washburn et al. 1977; Crabtree et al. 1978; Theroux and 
Long 1978; Denton and Theroux 1979; Flavell 1979; Hard et al. 1979; Long and Theroux 1979; 
Pettinger and Johnsey 1979; Page et al. 1980, 1982; Ismail 1981; Niwa and Hard 1981; Ismail and 
Long 1982; Niwa 1982; Nathanson et al. 1985; Niwa et al. 1986). However, as it turned out, the "big 
bug" proposal was shelved to allow an expanded biological control effort to bear fruit. 


At the Pacific Northwest Forest Research Experiment Station's (PNW) Corvallis Laboratory, R.B. 
Ryan drafted a study plan that called for the introduction of parasite species in addition to A. pumila. 
Because of the considerable time already invested in the single-species parasite introduction 
approach, additional species were to be added to some plots while maintaining the Agathis-only 
character of others. That would permit a few establishment foci from which additional parasite 
species could spread and assist in biological control, while at the same time allow data to be gathered 
on the single-species vs. multiple-species polemic. Those two types of plots plus a check plot (with 
no introduced parasites) were to be established in each infested state. Participants in the study agreed 
to gather the appropriate data from the three plots, constituting a block, in their area of responsibility, 
i.e. INT in Idaho, Region 1 Forest Pest Management in Montana, Region 6 Forest Pest Management 
in Washington, and PNW in Oregon. It was difficult in Idaho, Washington and Montana to establish 
check plots to conform to the arbitrary 50 miles between plots because of the widespread releases in 
those states of A. pumila in the 1960s. Nevertheless, check plots were established as far from 
previous releases as possible. Distance to previous release plots was not a problem in Oregon, 
because it had not been infested at the time and no releases of A. pumila had been made in that state. 


In addition to stock of A. pumila and C. laricinellae from the eastern U.S., releases in the western 
infestation originated from collections in numerous localities in Europe and Japan. Adults were 
received through the Canadian Quarantine Stations at Belleville, Ontario (1971-72) and Ottawa 
(1973), and the USDA-ARS station at Newark, DE (1974-80). Between 1971 and 1982, releases 
included the four species previously released in the eastern U.S., namely A. pumila, C. laricinellae, 
D. westwoodii, and D. laricinellum, plus two other parasites from Europe, Elachertus argissa and 
Necremnus metalarus, and one from Japan, Dicladocerus japonicus (Denton 1972, 1979; Ryan and 
Denton 1973; Ryan et al. 1975, 1977; Ryan 1979c, 1981; Otvos and Quednau 1984; Coulson et al. 
1988). The following table lists the total numbers of each species released in the West from 1960-83: 


Agathis pumila 42,344 
Chrysocharis laricinellae 19,111 
Dicladocerus westwoodii 4,610 
D. japonicus 8,426 
Diadegma laricinellum 11,068 
Elachertus argissa 6,196 
Necremnus metalarus 13,184 


442 


These totals do not include the prodigious numbers of A. pumila and C. laricinellae redistributed 
from initial establishment sites (Bousfield et al. 1974; Ryan et al. 1977; Valcarce and Lowe 1980; 
Ebel et al. 1982; Thier 1982). 


Aside from the field-cage rearing to obtain adult A. pumila in 1964 and 1965S, all releases in the West 
were direct releases of adults obtained through quarantine or from laboratory cultures established 
from those adults. The latter was possible once the difficulties of culturing larch casebearer in the 
laboratory had been solved by learning how to manipulate its complex larval diapause and the 
availability of the deciduous larch foliage (Ryan 1975, 1979a and b). Culture of the parasites and 
further experimentation were then relatively easy (Ryan and Yoshimoto 1975; Ryan 1980). Because 
many of the releases were from laboratory cultures, they could be timed appropriately. There were 
recoveries soon after release of all of the species except N. metalarus. Elachertus argissa was 
recovered 15 miles from the nearest release after at least two field generations (Pettinger and Johnsey 
1979). However, only C. Jaricinellae spread and increased significantly to supplement the control 
value of A. pumila already established. Chrysocharis laricinellae was found at release sites, but also 
at other sites, suggesting an earlier establishment (Ryan et al. 1974; Ryan and Theroux 1981). 


The numbers of adults released were deemed adequate for E. argissa and N. metalarus which are 
uniparental (Ryan 1980). However, larger numbers of D. westwoodii, D. japonicus, and D. 
laricinellum, may have made establishment of those species more likely. Unfortunately, laboratory 
cultures of those species had to be terminated when Ryan was transferred in 1983 from Corvallis to 
La Grande, OR. 


Data were gathered for several years from the single-species vs. multiplespecies study. However, an 
epidemic of Douglas-fir tussock moth in the 1970s caused a change in priorities, and larch casebearer 
plots were neglected for several years in Washington and completely in Montana after 1974. In 
addition, the Agathis-only plot in Oregon was sprayed in 1974 with DDT to control Douglas-fir 
tussock moth and the population of A. pumila established there disappeared. Plots in Idaho were 
studied by Denton (1972-73) and R.F. Schmitz (INT) (1974-76) until Schmitz transferred out of the 
region in 1976. Several Idaho plots were studied for several more years by G.E. Long (Washington 
State University) and his students (Ismail 1981; Ismail and Long 1982; Long 1988, 1990; Ramsay 
and Long 1988). However, the original study design was abandoned. In Oregon, parasite evaluation 
continues to be a major focus, both in the original and in additional plots, but by using "before and 
after" and life-table methods (Ryan 1983, 1985a, b, and c, 1986, 1988, 1990; Ryan et al. 1987, 1989). 
Population dynamics and modeling research has been a large part of the larch casebearer research 
elsewhere as well (Brown and Kulhavy 1978a and b; Long 1988, 1990). 


Evaluation of the Oregon population published to date (1993) spans 18 years. The emphasis on 
evaluation of biological control of the larch casebearer represents a significant departure from some 
past biological control efforts in which evaluation was neglected. Populations of the larch casebearer 
are now (1993) much below what they were in the 1960s and 1970s, indicating successful biological 
control. In the years before casebearer populations decreased, feeding damage caused tree-growth 
losses in the western states estimated to equal a stumpage value of $3 million per year. With the 
reduced populations normal tree growth has returned (Ryan et al. 1989). Detailed analysis of 
life-table data from the Blue Mountains of Oregon identified the introduced parasite, A. pumila, as 
the key factor associated with the reduced populations there (Ryan 1990). In Montana and Idaho, 
where C. laricinellae appears to be much more important than in Oregon (Tunnock and Ryan 1985), 
the situation may have been somewhat different. However, no life-table work was conducted there. 


Research on the larch casebearer has furnished at least one valuable spin-off result. Chrysocharis 


laricinellae, although introduced for control of larch casebearer, parasitizes some other casebearer 
species as well. It became a key factor in the population dynamics of the pistol casebearer (LeRoux 


443 


et al. 1963: LeRoux 1971; Paradis and LeRoux 1971). Overall, the larch casebearer stands as one of 
the most successful and one of the most well-documented cases of biological control. 


9. Larch sawfly, Pristiphora erichsonii (Hartig) (Hymenoptera: Tenthredinidae). By Mary Ellen 
Dix 


The larch sawfly, one of the most serious pest of larch in North America, is native to Europe and 
Asia (Ives 1976). This sawfly has few native enemies in North America and most of these are not 
effective at managing sawfly damage. In 1910, an ichneumonid parasite from England, Mesoleius 
tenthredinis, was successfully introduced and established in Manitoba and Minnesota (Hewitt 1912). 
This parasite develops internally in the sawfly larvae and prepupae. In 1944, sawflies resistant to M 
tenthredinis were discovered in Manitoba (Muldrew 1953; Lejeune and Hildahl 1954). The same 
apparent "resistance" and low parasitism rate was observed in larch sawfly from northern Minnesota 
during 1947 to 1949. In 1952, A.T. Drooz found sawfly cocoons from Minnesota containing 
encapsulated eggs of the parasite (Drooz 1953). Between 1957 and 1973, Drooz documented the 
change in the distribution of resistant and susceptible sawflies in Minnesota, Wisconsin, Michigan, 
Illinois, Maine, Maryland, New York and Pennsylvania (Drooz 1957, 1975). 


During the early 1970s, a second ichneumonid parasite from Europe, Olesicampe benefactor, was 
released in Minnesota and Canada (Kulman et al. 1974). Oleisicampe benefactor was known to be 
effective in suppressing larch sawfly populations in Europe (Turnock and Muldrew 1971; Kulman et 
al. 1974). In April 1975, approximately 2,000 parasitized cocoons were shipped from Minnesota to 
North Carolina. The wasps were allowed to emerge and mate before they were released in 
Pennsylvania to control a severe larch sawfly outbreak. Oleiscampe benefactor parasitized 5% of the 
sawflies after four years; parasitism doubled annually for the next three years and reached 59% by 
the eighth year after release (Drooz et al. 1985b). 


10. Spruce budworm, Choristoneura fumiferana (Clemens), and western spruce budworm, C. 
occidentalis Freeman (Lepidoptera: Tortricidae). By Mary Ellen Dix and Leah S. Bauer 


Several species of budworms (Choristoneura spp.) are native to North America and over centuries 
have periodically caused extensive defoliation in spruce-fir and pine forests (Baskeville 1975; 
Harvey 1985). Two species, the spruce budworm (SBW; often called "eastern spruce budworm") and 
western spruce budworm (WSBW), are of major economic importance in both the U.S. and Canada 
(Blais 1985; Harvey 1985; Shepherd 1985). Research on the biological control of budworms was 
conducted by both federal and university scientists and can generally be divided into three phases: 
pre-CANUSA, CANUSA, and post-CANUSA. 


Pre-CANUSA. The pre-CANUSA (1943-1976) era of budworm biological control research 
emphasized identification of natural control agents, documentation of biological aspects, and 
microbial control trials. Before 1953, USDA Bureau of Entomology and Plant Quarantine (BEPQ) 
scientists identified natural enemies, determined their impacts, and documented aspects of their 
biologies in New York (Dowden et al. 1948; Dowden and Carolin 1950), Maine (Jaynes and Drooz 
1952; Dowden et al. 1953), and Colorado (Dowden et al. 1948). George and Mitchell (1948) 
estimated that birds ate 3.5 to 7.0% of the SBW. Dowden et al. (1953) analyzed the stomach contents 
of red squirrels, and was able to demonstrate that birds ate larger quantities of budworms than do red 
squirrels. In a Michigan survey, Mattson et al. (1968) and Mattson (1974) also demonstrated that 
birds were more important predators than mammals in regulating budworm populations. Several of 
the scientists who worked for BEPQ in Maine, New York, and Colorado later joined the Forest 
Service and formed the core of the spruce budworms research effort. 


444 


During the pre-CANUSA period, budworms also severely defoliated Canadian forests. 
Consequently, most Canadian biological control research also focused on identification of parasites, 
parasitoids (parasites that kill their hosts), predators, and microbial pathogens, and related studies on 
the biologies, life cycles, alternate hosts, and impacts of these natural enemies (McKnight 1968). 
During the 1960s, the focus of Forest Service biological control research shifted toward the use of 
microbials, and away from other natural controls. Canadian research continued to focus on parasites 
and predators. 


McKnight (1971) studied WSBW outbreaks in the central and southern Rocky Mountains and 
reported that natural controls appeared to regulate most WSBW populations. Insect parasites of the 
WSBW were identified and their abundance and distribution determined for Colorado (McKnight 
1974), Montana (Williams et al. 1969), and Oregon (Carolin and Coulter 1959). Carolin and Coulter 
(1959) also evaluated the impact of parasitism and hyperparasitism on WSBW outbreaks. 
Entomologists in the Pacific Northwest Experiment Station (PNW) used the greater wax moth as a 
host for intensive laboratory studies of Ephialtes (as Apechthis) ontario and Itoplectis 
quadricingulata, two solitary ichneumonid pupal parasites of WSBW and hemlock looper. These 
studies determined that photoperiod affected parasite diapause, higher host densities were more 
favorable to parasite abundance, and that a silken cocoon increased parasite larval survival (USDA, 
Forest Service 1968). 


CANUSA. The Canada-United States Spruce Budworms Research and Development Program 
(CANUSA) was formed in 1977, when Robert Berglund (U.S. Secretary of Agriculture) and Romeo 
LeBlanc (Minister of Environment Canada) signed a six- year expanded and accelerated research and 
development effort. The broad objective of the cooperative agreement was to design and evaluate 
tactics and strategies for not only controlling spruce budworms, but also managing budworm-infested 
forests in an economically and environmentally acceptable manner (Grimble and Lewis 1985; 
Winget 1985). This agreement expanded research on microbial control of spruce budworms and 
increased research efforts on parasites. Melvin E. McKnight was the Program Leader for the U.S. 
The Forest Service program was coordinated by an Eastern Region Program Manager, Dan M. 
Schmitt at Broomall, PA, and a series of Western Region Program Managers at Portland, OR (Max 
W. McFadden, Ronald Stark, and James Colbert) (Buckner and McKnight 1985). Although much of 
CANUSA research focused on the development and demonstration of management techniques 
including pesticides, considerable research was also conducted on natural enemies of both SBW and 
WSBW. In the Northeast, D.T. Jennings, an entomologist, and H.S. Crawford, a wildlife biologist, 
organized SBW natural enemy research for the Northeastern Forest Experiment Station (NE), Orono, 
ME. In the Pacific Northwest, T.R. Torgersen and R.R. Mason, entomologists at the PNW station at 
LaGrande, OR, led research on the WSBW. Because much of this research continued after 
CANUSA, the discussion is summarized in separate sections below on parasite, predator, and 
pathogen research. 


One goal of CANUSA was to catalogue all available information on spruce budworms including 
their natural enemies. Literature was compiled and a bibliography and several supplements were 
published (Jennings et al. 1979, 1981, 1982; McKnight et al. 1988). These bibliographies included 
publications on biological control research on SBW and WSBW throughout North America. The 
University of Maine and the Canadian Forest Service at Fredericton, New Brunswick, are continuing 
these efforts (White 1992). In September 1984, at the end of CANUSA, a CANUSA Budworms 
Research Symposium was held in Bangor, ME. The symposium brought together all budworm 
researchers and produced a summary publication describing their research advances (Sanders et al. 
1985). Also, a comprehensive summary of available information on all predators and potential 
predators of each stage of SBW was published (Jennings and Crawford 1985). 


445 


Post-CANUSA. Although special funding for budworm research ceased after 1983, research on 
predators and pathogens continued in the Northeast and Pacific Northwest. Jennings and Crawford 
continued to lead research efforts on SBW in the Northeast, while Torgersen, Mason, and R.W. 
Campbell worked on the WSBW in the Northwest. In the northeast, long-term research goals were 
directed toward development of techniques for the conservation and enhancement of key natural 
enemies (Jennings et al. 1984, 1986, 1990a and b, 1991). These included studies on the roles of birds, 
ants, trap-nesting wasps, phalangids, small mammals, parasitic and predaceous mites, and spiders in 
the population dynamics of the SBW to develop effective techniques for manipulating predator 
populations (Crawford 1985; Crawford and Jennings 1985, 1986; Houseweart et al. 1980; Jennings 
and Crawford 1983, 1985, 1989; Jennings and Houseweart 1978; Jennings et al. 1984, 1986, 1990a 
and b, 1991). Other researchers in the PNW designed studies to develop more effective pathogens 
and delivery systems. In 1988, funding for research on arthropod predators of SBW ceased at Orono, 
ME, and Jennings was transferred to Morgantown, WV, to work on gypsy moth predators. 


In the late 1980s and early 1990s, Campbell synthesized research results from studies on SBW and 
WSBW, and developed a comprehensive model of budworm population dynamics. The role of 
natural enemies, especially avian and ant predators, was discussed in his compendium (Campbell 
1993). 


Parasite research. The chalcidoid Trichogramma minutum parasitizes eggs of both SBW and WSBW 
shortly after the eggs are laid on the host tree foliage in early summer. Generally, less than 15% of 
the eggs are parasitized, and hence this species has not been considered an important factor in 
regulating budworm populations (Miller 1953, 1963; McGugan and Blais 1959; Neilson 1963; 
Thomas 1966). However, some scientists believe that Trichogramma spp. have good potential as 
augmentative biological control agents and have inundated agroecosystems with species of this egg 
parasitic genus (DeBach and Hagen 1964; Ridgway et al. 1981). Researchers have successfully 
released Trichogramma spp. in Canada. Papers that describe these releases can be found in the White 
(1992) supplement to the SBW bibliography. 


In Maine and Canada, both U.S. and Canadian Forest Service scientists and their cooperators 
collected data needed to develop a mass-release program for 7. minutum. This parasite was mass- 
reared on eggs of Angoumois grain moth. Parasites emerging from grain moth eggs were found to be 
smaller than those reared from SBW eggs (either laboratory- or field-reared). The size difference 
rapidly reversed when the parasites were subsequently reared on SBW eggs (Southard et al. 1982). 
However, mean daily production of the parasite on the grain moth was higher than on SBW 
(Houseweart et al. 1983), and the parasite also developed faster in grain moth than on SBW eggs. 
Because of the parasite's short development time, parasite progeny could be released early in the 
SBW's oviposition period (Lawrence et al. 1985). Houseweart et al. (1982) evaluated the 
acceptability and availability of SBW eggs to the parasites and found that female 7. minutum 
preferred SBW eggs that were one to three days old. Jennings and Houseweart (1983) found that the 
parasite preferred budworm egg masses that were already parasitized by T. minutum. 


Between 1977 and 1981, Houseweart et al. (1984) conducted a series of field releases of T. minutum 
in Maine. The commercially-reared California strain of 7. minutum was released in 1977. However, 
this commercial strain was not as successful a control agent as Maine-reared 7. minutum that were 
released in 1978, 1979 and 1981. Broadcast and multiple releases from the ground in 1979 were 
slightly more effective than the four-point releases in 1978. Three closely- timed aerial releases of T. 
minutum in 1981 were the most effective releases; however, none were successful in regulating. . 
epidemic populations of the SBW (Houseweart et al. 1984). 


The ichneumonid Glypta fumiferanae, an important larval endoparasite of WSBW, diapauses in 
overwintering second-instar host larvae. Shon and Shea (1976) successfully reared one generation of 


446 


non-diapausing male progeny on non-diapausing hosts. Rappaport and Page (1985) developed a 
technique for rearing G. fumiferanae on five successive generations of non-diapausing WSBW in the 
laboratory. 


In order to determine the effects of insecticides on budworm parasites, Schmid (1981) evaluated the 
distribution of the parasites within the tree. He found that parasitism did not differ among sides of the 
tree or crown levels of the host. Thus, sampling at levels or sides of the tree could be used to estimate 
total parasitism. Total percentage parasitism for most parasite species changed insignificantly during 
the two years following insecticide application, but percentages for each species varied with site and 
year. 


The CANUSA Spruce Budworms program also supported research on the role of parasites in WSBW 
‘population dynamics in the western U.S. and Canada. Torgersen et al (1984b) examined the 
relationships of parasitism to variation in budworm survival rates over a range of population densities 
in widely scattered areas. They found that parasitism contributed little to the variation in survival 
rates from fourth-instar larvae to adults or within generations. Parasites were slow to respond to 
increases in available hosts. They concluded that parasitization played a smaller role in budworm 
population dynamics than previously suspected (Campbell and Torgersen 1983a; Torgersen, et al. 
1984b). 


Predator research in the Northeast. In 1976, Crawford, Jennings and cooperators initiated a series of 
studies to identify vertebrate predators of SBW and determine their distribution and impact on SBW 
populations in the Northeast (Crawford and Jennings 1985). A literature review and annotated 
bibliography on relationships between birds and SBW, and a summary of available information on 
predators of each SBW life stage were published (Crawford and Jennings 1982; Jennings and 
Crawford 1985). 


Jennings, Crawford, and cooperators identified birds commonly found in SBW outbreaks and 
determined their diet through visual observation and gut analyses. For example, they observed pine 
siskins consuming SBW egg masses (Jennings and Crawford 1983) and calculated that birds ate 
2.4% of large SBW larvae and pupae in Maine and New Hampshire (Crawford et al. 1983). Crawford 
and Titterington (1979) found that forest stands composed primarily of balsam fir had an 
impoverished avifauna and that mixed stands of spruce and fir supported increased bird populations. 
Furthermore, abundance of canopy-frequenting warblers and golden-crowned kinglets varied with 
changes in composition of the spruce-fir stand (Crawford and Titterington 1979; Titterington et al. 
1979). Unmanaged even-age fir stands of pole or small sawlog size balsam fir were found to be poor 
bird habitat and were usually more susceptible to SBW infestation and damage than non- 
homogeneous stands. Conversely, management of uneven-age stands enhanced habitat for birds that 
prey on SBW (Crawford and Jennings 1986). Based on these results, silvicultural practices were 
recommended for increasing avian populations of budworm predators by manipulating tree species 
and stand diversity (Crawford and Titterington 1979; Titterington et al. 1979). 


During the 1980s, research efforts continued to target the role of birds in regulating SBW 
populations. The bird species that preyed on SBW in sparse, transitional and outbreak SBW 
populations were evaluated (Crawford and Jennings 1985), and the hypothesis that birds may restrict 
expansion of low-density SBW populations was examined (Crawford and Jennings 1989). However, 
Campbell (1985) found that birds had little or no effect on sparse SBW populations in New York. 
Crawford et al. (1990) suggested that early increases in SBW populations could be detected by the 
number of SBW larvae in the stomach contents of red-breasted nuthatches. 


447 


During the bird studies, the digestive tracts of red squirrels were also examined; it was found that 
less than 6.7% of the squirrels ate budworms indicating that squirrels were minor predators of SBW 
(Jennings and Crawford 1989). 


Spiders, ants, phalangids (Opiliones), eumenine wasps, mites, carabids, and other invertebrates that 
prey on SBW also may play a role in regulating the SBW populations. However, in the mid-1970s, 
the identity of the predaceous species, and their impact and biologies, were unknown or poorly 
understood. In 1976, Jennings and his CANUSA cooperators initiated a series of studies to identify 
invertebrate predators in the different northeastern forests, determine their distribution and densities, 
and assess their impacts. Visual observations of actual feeding and prey capture in webs, stomach- 
content analyses, and examination of provisions in trap-nesting blocks, were all used to document 
predation. Jennings and M.W. Houseweart (University of Maine, Orono) reported egg predation by 
male jumping spiders (Jennings and Houseweart 1978). Jennings and Crawford (1985) and Jennings 
and Collins (1987) identified web-spinning spiders that prey on SBW by visually observing prey in 
their webs. Web-spinners were found to be more abundant than hunting spiders on red spruce 
(Jennings and Collins 1987) and were the most abundant spider species caught in malaise traps 
deployed in the spruce-fir forests of west-central Maine (Jennings and Hilburn 1988). By 1989, 
Jennings and Houseweart had identified 15 species of spiders in 12 genera of six families that prey 
on SBW moths. Nine of those species appeared to prefer male moths to females (Jennings and 
Houseweart 1989); it was speculated that this sex-biased predation was due to sex-pheromone 
mimicry, uneven prey densities, accidental captures, moth behavior, and moth-flight activity. 


Because first, second and later instar larvae of the SBW often drop to the forest floor, spiders living 
on the forest floor are also potential SBW predators. Jennings and cooperators used formalin to 
extract spiders from sublitter habitats on the forest floor. They found that most spiders were 
associated with one or two forest-stand types (Jennings et al. 1990b) and represented species that had 
been collected previously in pitfall traps deployed in spruce-fir forests (Jennings et al. 1988; Hilburn 
and Jennings 1988). 


Jennings and Dimond (1988) described the arboreal spider fauna associated with balsam fir and 
spruces in Maine, compared spider-SBW densities among sampling sites, and explored possible 
relationships between spiders, budworms, and forest stand parameters. They found dissimilarities 
among sites and between foraging strategy (web-spinner, hunter) and that host tree species affected 
spider densities. Spider densities per m’ of foliage area generally were greater on spruces than on 
balsam fir. They further hypothesized that because the percentage of particular tree species in a stand 
affects overall estimates of spider densities, spider densities could perhaps be managed through 
silvicultural manipulation of tree species composition. 


Jennings et al. (1984) identified the phalangid fauna of strip-clearcut and dense spruce-fir forests 
infested with SBW, and determined their relative abundance among replicated forest conditions, 
seasonal activities, and species richness and diversity. They found significantly more phalangid 
individuals and species in uncut residual stands and in dense stands than in clearcut strips. 


Jennings et al. (1986) identified ant species associated with strip-clearcut and dense forests of 
northern Maine, and found that the ants were not more or less abundant in any particular forest type, 
and that ant species density varied between years and sites. 


Jennings and cooperators at the University of Maine identified the solitary trap-nesting vespid wasps 
of the subfamily Eumeninae that provisioned nesting blocks with SBW in strip-clearcut and dense 
spruce-fir forests of northern Maine (Jennings and Houseweart 1984; Collins and Jennings 1987a and 
b). The preferred nest height of the wasps was also determined. Among provisioned lepidopteran 
prey, SBW accounted for 3 to 94% of the stocked larvae, with SBW stocking levels in the nests’ 


448 


apparently dependent on local SBW abundance (Jennings and Houseweart 1984; Collins and 
Jennings 1987a). Some eumenine predators from the western U.S. were released in Maine in 1983 
(Coulson 1994). 


Mites are both predators and parasites of SBW in northeastern spruce-fir forests (Houseweart et al. 
1980; Jennings and Crawford 1985; Welbourn and Jennings 1991). Welbourn and Jennings (1991) 
described two new species of erythraeid mites. Houseweart et al. (1980) found mites on up to 28% of 
the male moths collected in pheromone traps and on similar percentages of free-flying moths, and 
concluded that parasitism by mites could affect moth flight behavior. 


Many species of carabid beetles are known to prey on arthropods, and many carabid species were 
common in northeastern spruce-fir forests. Krall and Simmons (1978) identified nine species preying 
on SBW larvae by tagging the SBW larvae with phosphorus-32 and tracing the radioisotope to the 
carabid predators; the carabid Prerostichus adstrictus accounted for most of the predation in Maine. 
Reeves et al. (1983) used barrier-pitfall traps and tree bands to identify carabid beetles in forests of 
northern New Hampshire. . 


Predator research in the West. In 1979, Torgersen, Mason and Campbell initiated a series of studies 
on the population dynamics of the WSBW. During the next 12 years, they used artificial stocking 
techniques, specialized prey-census methods, selective enclosures, and sticky barriers to identify and 
quantify bird and ant predation on WSBW (Torgersen et al. 1990). They found that predators killed 
about 95% of the WSBW (Campbell and Torgersen 1982) and that birds and foliage-foraging ants 
were the dominant predators of WSBW larvae and pupae in the northwestern U.S. Youngs and 
Campbell (1984) identified ten species of ants that prey on WSBW. Information on the identity and 
distribution of ants preying on WSBW in Oregon and western Montana was published (Youngs and 
Campbell 1984; Youngs 1985). Two species, the western thatching ant and a Camponotus species, 
were found on one-third of the trees surveyed. Shattuck (1985) developed an illustrated key to ants 
associated with the WSBW, which enabled pest managers to identify the common species. Based on 
results obtained from enclosures and traps that excluded birds (single branch exclusion cages, entire 
tree cages, and sticky traps), ants were the most important predator of WSBW (Campbell and 
Torgersen 1982). Torgersen and Campbell (1982) also used single branch enclosures to determine 
effects of avian predators on WSBW, and found densities of WSBW influenced levels of bird 
predation. Garton et al. (1985) demonstrated that forest birds consume large numbers of WSBW, and 
concluded that manipulating the ecosystem to increase bird diversity could be an economical method 
to manage WSBW. 


In Montana, Carlson et al. (1984) found that infested young Douglas-fir and western larch trees had 
higher WSBW densities if they were protected from birds and ants during the fourth larval instar 
through the pupal stage of the pest. Campbell et al. (1984) found that both birds and ants reduced 
WSBW populations on western larch seedlings, while ants appeared to be more important on 
Douglas-fir seedlings. At high budworm densities, neither ants nor birds significantly reduced 
WSBW densities, from larvae to adults. However, at low host densities, ants alone caused about a 
five-fold reduction in WSBW survival, when compared to high host densities. Birds alone permitted 
about 8% survival of WSBW, causing about a six-fold reduction in survival, compared to WSBW 
survival at high densities. They concluded that ants were the more important predator (Torgersen 
1985a). 


Campbell and Torgersen (1983b) found that birds and ants appeared to partition the crown strata. 
Ants were more effective at the lower levels, while birds were effective throughout the crown. 
Because both bird and ant populations were influenced by availability of standing and dead wood, 
they recommended the retention of snags to provide habitat for ant and bird populations. Current 
(1993) research at the PNW Station addresses the role of standing and downed dead-wood as colony 


449 


substrate for foliage-foraging ant predators of WSBW. A related study in northeastern Oregon is 
assessing predation of these ants by pileated woodpeckers. A long-term study is aimed at identifying 
and quantifying arboreal spiders that prey on WSBW, determining spider density and diversity in 
different forest environments, and assessing how their effectiveness as natural enemies is affected by 
forest management practices. 


During a 1983 WSBW-suppression project, Murphy (1985) examined the effects of aerial application 
of carbaryl on predaceous ants. He found that ant populations were suppressed with carbaryl use, 
which was potentially detrimental to overall WSBW management. 


Pathogens. The bacterium Bacillus thuringiensis (Bt) was originally isolated from silkworms in 1901 
(Cunningham 1985). In 1960, the first large-scale field tests of commercially-produced Bt were 
conducted against SBW outbreaks in New Brunswick, Canada (Mott et al. 1961). R.E. Denton 
(Intermountain Station [INT], Ogden, UT) showed that Bt was toxic to WSBW larvae in the field and 
laboratory, when sufficient amount of toxin was ingested (Denton 1960). In 1963, W.H. Klein (INT, 
Ogden, UT) and F.B. Lewis (NE, New Haven, CT) applied a new formulation of Bt with a helicopter 
to a SBW infestation in balsam fir-spruce stands of northern Maine. They found that Bt was not as 
effective as conventional pesticides in reducing SBW populations (Klein and Lewis 1966). 


During the 1960s and 1970s, Bt formulations and application technology steadily improved. Between 
1968 and 1980, Bt was used in operational spray projects in the Northeast, especially in Maine (Trial 
1985). In 1978, the first guidelines were formulated for operational use of Bt (Morris 1980). 
Although Bt suppressed SBW populations, field tests and projects often had inconsistent results and 
were thus inconclusive. In 1972, 1973, and 1974, the effectiveness of Bt in reducing SBW 
populations was evaluated in northern Maine by J.B. Dimond (University of Maine). The results of 
the aerial application of Bt alone, combined with other insecticides, and combined with a chitinase 
additive were all inconclusive (Dimond 1975). 


In 1975, a State and Private Forestry pilot test in western Montana evaluated impacts of aerially- 
applied Bt on WSBW populations, foliage damage levels in the year of treatment and the following 
year, and impacts on parasite abundance. M.D. McGregor and colleagues (State and Private Forestry, 
Northern Region, Missoula, MT) reported significant reductions in WSBW larvae, but with minimal 
foliage protection and disruption of parasite populations; they suggested that Bt did not impact the 
parasites directly but disrupted their life cycle in the host (McGregor et al. 1976). Thompson et al. 
(1977) reported that immatures of the WSBW parasites Glypta fumiferanae and Apanteles 
fumiferanae can obtain a lethal dose of Bt from infected WSBW. 


In 1980, CANUSA sponsored a field test to determine the efficacy of two aerially-applied 
commercially-available Bt (HD-1) formulations in northern Wisconsin, New Hampshire and Maine. 
SBW populations and defoliation were successfully reduced in Wisconsin using Bt (Reardon et al. 
1982). In 1981, R.C. Reardon (Pacific Southwest Station [PSW], Davis, CA) and K. Haissig 
(Wisconsin Department of Natural Resources, Rhinelander) observed lower SBW densities and less 
defoliation of balsam fir in treated plots in Wisconsin, even though the Bt did not persist (Reardon 
and Haissig 1983). Dimond (1985a) reported negative results in Maine. Another 1981 study in 
Wisconsin also obtained baseline data on Bt persistence at different dosages following ground 
applications with a mist blower. SBW were killed for up to 16 days post-spray and viable spores 
were collected on white spruce for up to a year post-spray (Reardon and Haissig 1984). In the mid- 
1980s, a cooperative study by State and Private Forestry (Northeastern Area, Durham, NH) and the 
Passamaquoddy Indian Tribe successfully reduced SBW populations on the Passamaquoddy 
reservation in Maine (McCreery and Francis 1984; McCreery et al. 1985). 


450 


Pilot tests in northern New Mexico (1981-82) and central Montana (1981) demonstrated that Bt can 
reduce WSBW populations and damage levels (Ragenovich 1983; Stipe et al. 1983). In 1985, Bt 
successfully reduced WSBW in Carson National Forest in New Mexico (Rogers 1992). 


In 1984, field efficacy and persistence of the HD-1 Bt strain was compared to a new NRD-12 strain 
in Oregon (Beckwith and Stelzer 1987; Stelzer and Beckwith 1988). The NRD-12 strain is 
serologically similar to the HD-1 strain, but killed gypsy moth larvae faster than the HD-1 strain 
(Dubois 1985a and b; Stelzer and Beckwith 1988). Aerial application of both strains successfully 
reduced WSBW populations, with similar efficacy. The 30 billion International Units (BIU) in spray 
volume of 7.1 liters/hectare rate was more effective than a 20 BIU rate (Stelzer and Beckwith 1988). 


Studies at the Univerity of Massachusetts involved screening of 402 strains of more than 18 Bt 
varieties. The investigators found a strong correlation between enhanced lethality to SBW and 
chitinase titre within the serovar; strains grown with chitinase produced a faster kill rate (Gunner et 
al. 1985). 


Niwa et al. (1987) evaluated interactions of Bt with parasites in the field tests and found no 
differences in parasitism and species distribution between control and treatment plots. Although they 
found Bt in three parasite species, they concluded that Bt was not detrimental to the associated 
parasite complex (Niwa et al. 1987). 


By 1985, Bt had changed from a little-used, expensive material of questionable reliability to one that 
could compete favorably with chemical insecticides. This was due in part to the identification of 
more potent strains as well as CANUSA and gypsy moth program-sponsored research aimed at 
improved formulations, dosage rates, and application technologies (Dimond et al. 1981; Dimond 
1982, 1985a and b; Reardon et al. 1982; Walton and Lewis 1982; Morris 1982; Grimble and Morris 
1983; Fast and Dimond 1984; Reardon and Haissig 1984; Gunner et al. 1985; Dubois 1985b; 
Beckwith and Stelzer 1987; Niwa et al. 1987; Stelzer and Beckswith 1988). Morris et al. (1984) 
published improved guidelines for the operational use of Bt against SBW that were based on the 
results of CANUSA research. 


The Bt Meacham Pilot Study was initiated as part of the 1988 Western Spruce Budworm Operational 
Suppression Project for Washington and Oregon. This study compared ultra-low-volume (ULV) 
aerial applications of Dipel™ and Thuricide™ formulations with untreated controls (Torgersen et al. 
1994). Mason et al. (1989) published a model using linear regressions for estimating mid-crown 
densities of WSBW using lower-crown samples. Entomologists of the PNW station at LaGrande, 
OR, assessed the relationship between late-instar WSBW larval abundance in the lower-crown and 
mid-crown of Bt-treated trees. They found no difference in WSBW densities between crown levels 
over time and concluded that lower-crown sampling was quick, inexpensive and accurate (Torgersen 
et al. 1994). Workers at the NE station at Morgantown, WV, are currently (1993) developing a model 
for converting lower-crown samples to mid-crown densities in natural populations of WSBW. 


Research also is continuing on the long-term impacts of Bt on the WSBW population dynamics and 
the ULV Bt Meacham Pilot Study. In addition, effects of Bt on non-target Lepidoptera, food for the 
Townsend's long-eared bat, are being characterized in Oregon (unpublished internal Forest Service 
Report). With the development of plant biotechnology and molecular biology, researchers have 
transfered Bt 6-endotoxin genes into Douglas-fir. Tree tissue was then bioassayed for toxicity in 
SBW (Beckwith et al. 1988). Plant genetic engineering may be a useful tool in the development of 
pest-resistant transgenic trees. 


Much of the developmental virus research on SBW was conducted in Canada and later applied in the 
U.S. Nuclear polyhedrosis (NPV) and granulosis (GV) viruses of the SBW were first reported in 


451 


Canada by Bergold (1950) and Bird and Whalen (1954), respectively. Field tests of the NPV and GV 
produced mortality in both 1959 and 1960 (Stairs and Bird 1962). Cunningham et al. (1972) 
developed a method for mass-producing two viruses of SBW in Canada and a number of Canadian 
researchers developed the technology for producing and applying viruses (Cunningham 1985). Aerial 
applications of both viruses against SBW in eastern Canada have occurred since 1971 (Cunningham 
et al. 1980; Cunningham et al. 1983a and b). However, in the West, the distribution of natural 
epizootics of NPV and GV in WSBW are limited to a few isolated patches and have been rarely 
reported in outbreak populations. Researchers at the PNW stations at Corvallis and Portland, OR, 
found that NPV and GV applied on grand fir reduced WSBW larval populations to acceptable levels 
by protecting 35% of the new foliage (Stelzer and Scott 1985). 


Alternate hosts that are easy to study in the laboratory were needed to evaluate viruses. Stairs et al. 
(1981) fed an isolate of a NPV from SBW to neonate larvae of the cabbage looper and the greater 
wax moth. The larvae of these species were successfully infected, demonstrating that alternate hosts 
could be used to study the virus. 


Microsporida are obligate intracellular protozoans, the causal agents of ubiquitous and somewhat 
chronic disease of insect and other invertebrates. Nosema fumiferanae is the most common 
microsporidan parasite found in SBW, and in the field, the prevalence of this pathogen increases in a 
density-dependent manner with its host (Cunningham 1985). In 1983, Leah S. Bauer (North Central 
Experiment Station, East Lansing, MI) in collaboration with G.L. Nordin (University of Kentucky, 
Lexington) began research on the importance of this indigenous pathogen in the population dynamics 
of SBW. Bauer and Nordin (1988a) developed a reproducible laboratory bioassay for determining the 
pathogenicity (median lethal dosages and times) of N. fumiferanae via per os inoculation in fourth- 
and fifth-instar larvae. The sublethal responses included prolonged larval development, smaller 
pupae, and shortened adult longevity. They also quantified the impact of larval age, microsporidan 
dose, and diapause conditions on the lethal and sublethal responses of SBW to N. fumiferanae. Ina 
subsequent study, Bauer and Nordin (1989a) quantified a dose-dependent reduction in fecunditiy in 
SBW inoculated per os. In addition, N. fumiferanae was efficiently transmitted transovarially from 
mother to progeny. Infected progency experienced twice the larval mortality, and survivors took 
longer to develop and were 25% smaller than uninfected progeny. In a separate study the nutritional 
physiology of larvae infected with NV. fumiferanae was quantified in an effort to determine the 
mechanisms of disease (Bauer and Nordin 1988b). They found suppressed rates of food 
consumption, relative growth rate, and production efficiencies in SBW infected with N. fumiferanae. 
However, approximate digestibility and nitrogen utilization efficiency of food in diseased larvae 
were higher than in healthy larvae. Moreover, the lethal and sublethal responses of infected larvae 
fed on diet containing 4.5% nitrogen were significantly less that cohorts reared on 2.5% dietary 
nitrogen. Bauer and Nordin (1989b) also determined that larvae, transovarially-infected N. 
fumiferanae, were more susceptible to Bt than healthy larvae. 


Since the completion of these studies in 1988, funding and interest in SBW population dynamics 
waned with the outbreak itself, particularly in the U.S. However, Canadian researchers, recognizing 
the repressive potential of N. fumiferanae on SBW populations, have established long-term studies 


aimed at quantifying its impact and incidence during periods of low population density (L.S. Bauer, 
personnel observation). 


In 1980, in cooperative University of California and PSW studies at Davis, CA, the nematode 
Steinernema carpocapsae with its associated bacterium Xenorhabdus nematophilus was applied to 
WSBW in the laboratory and field; results were inconsistent, probably because of the dessication and 
death of most of the nematodes (Kaya et al. 1981). The following year, the researchers compared 
four antidessicants as additives to the nematode solution. Because larval WSBW populations were 
still not significantly reduced, they recommended that application of nematodes be discontinued until 


452 


more effective techniques were developed for increasing nematode survival (Kaya and Reardon 
1982). 


E. Sap-Sucking Insects 
1. Balsam woolly adelgid, Adelges piceae (Ratzeburg). By Gene D. Amman 


The baisam woolly adelgid was accidentally introduced into the Maritime Provinces of eastern 
Canada and into the northeastern U.S. from Europe about 1900, presumably on infested nursery stock 
(Kotinsky 1916; Balch 1952). Subsequently, the adelgid was found in central California in 1928 
(Annand 1928), and severe outbreaks have occurred in Oregon and Washington since 1954 
(Whiteside 1955). Infestations were first seen in the Mt. Mitchell area of North Carolina in 1955 
(Kulman 1964). Movement of the adelgid to these areas also probably occurred on infested nursery 
stock. The balsam woolly adelgid is found principally on silver fir throughout western and central 
Europe, where it may be native. That host is not physiologically damaged by the adelgid, apparently 
because it is not sensitive to bark-infesting pests. All North American firs (Abies species) are 
susceptible to this adelgid. 


The balsam woolly adelgid is a very small, completely parthenogenetic homopteran. It is confined 
solely to true firs, unlike most adelgids which alternate between a primary spruce host and a 
secondary host in the family Pinaceae. Winged forms are rare, and may not exist at all in some 
populations. Dispersal is primarily during the first nymphal instar, when the adelgid actively searches 
the host tree for a suitable feeding site. The motile nymphs are frequently picked up by winds and 
dispersed over long distances. The adelgid has two to four generations per year, depending upon 
environmental conditions, and overwinters as an early first-instar nymph, which is extremely 
resistant to freezing. 


The use of chemical insecticides to control the adelgid over the large inaccessible areas infested by 
the pest was impractical. Therefore, the widespread mortality of trees prompted predator introduction 
programs to bring about some control. From 1957 through 1960, predators were collected in Europe 
and Australia by the Commonwealth Institute of Biological Control, and screened through the 
Canadian Department of Agriculture. Predators from Europe were also screened by ARS (USDA). In 
1958, P.B.Dowden (Northeastern Forest Experiment Station [NE], New Haven, CT) searched for 
predators in Japan. After 1960, predator introductions from India and Pakistan were financed by the 
Forest Service through Public Law 480, and were screened by the ARS quarantine facility in New 
Jersey. The success of introductions into Canada was discussed by McGugan and Coppel (1962a). 


New England. Predator introductions for control of the balsam woolly adelgid on balsam fir were 
under the overall direction of Dowden. David Crosby also participated in the work. The first 
introduction into the U.S. was unplanned, when the chamaemyid fly Leucopis obscura spread 
inadvertently into Maine, about 1937, from New Brunswick, where it had been introduced from 
England. Planned introductions of predators into the U.S. started in 1957 and continued through 1960 
(Dowden 1962). A total of 21,390 specimens, representing four species of predators, were introduced 
into Maine, Vermont, New Hampshire and New York (Table 2). Leucopis obscura and the 
derodontid beetle Laricobius erichsonii became established (Dowden 1962). Following 
establishment, 3,175 L. obscura were collected and released at additional sites in New Hampshire, 
New York and Vermont. Effectiveness of the introductions was not determined. However, the 
continued mortality of balsam fir caused by the adelgid suggests that they were not very effective. 


North Carolina. Predator introductions into North Carolina for control of the balsam woolly adelgid 


on Fraser fir in the Mt. Mitchell area were under the direction of G.D. Amman (Southeastern Forest 
Experiment Station [SE], Asheville, NC). Others involved with introductions and evaluations were 


453 


G.F. Fedde, C.F. Speers, and J.A. Witter. These introductions were started in 1959 and extended 
through 1966. The releases totaled 46,325 individuals of 22 species from Germany, Austria, 
Australia, New England (previously introduced from England), India, and Pakistan (see Table 3 for 
list of species) (Amman 1961; Amman and Speers 1964, 1971). Of this group, three species initially 
overwintered and reproduced successfully: the cecidomyiid Aphidoletes thompsoni and the beetles L. 
erichsonii and Aphidecta obliterata. However, in an extensive survey in 1968, only Laricobius was 
recovered (Fedde 1972). None of the predators from India and Pakistan were recovered following 
release. 


Oregon and Washington. Predator introductions into Oregon and Washington to control the balsam 
woolly adelgid on the regions's true firs (subalpine fir, Pacific silver fir, and grand fir) were under the 
direction of R.G. Mitchell (Pacific Northwest Forest Experiment Station [PNW], Portland, OR). 
Others involved with introductions and evaluations were K.H. Wright and P.E. Buffam. Predator 
liberations began in 1957 and continued through 1964. During this period, 19 species totaling 61,785 
specimens from seven countries were released (Table 4) (Mitchell and Wright 1967). These were 
only slightly more successful than those in the eastern U.S. Of this group, three species of flies (A. 
thompsoni, Cremifania nigrocellulata, and L. obscura) and two species of beetles (L. erichsonii and 
Scymnus [as Pullus] impexus) became established. Of the established predators, 1,562 Laricobius 
and 2,104 Aphidoletes were collected and recolonized in additional sites in Oregon and Washington. 
In addition to species released, four species from India and Pakistan were studied in the laboratory 
only. These were the coccinellids Ballia dianae and Oenopia sauzeti, and the neuropterans Chrysopa 
(sens. lat.) sp. and Hemerobius sp. 


Conclusions. Failure of the predators to establish was probably related to much cooler temperatures 
in all infested areas in the U.S. than in India and Pakistan on the lower slopes of the Himalayas, and 
in Europe, where the predators were originally collected. Failure of the introduced predators to 
accept the host plant as an oviposition site or the balsam woolly adelgid as prey are other possible 
factors contributing to their non-establishment, because many of the predators were collected from 
conifers other than fir, and original prey were often not Adelges species. None, with the exception of 
the anthocorid bug Tetraphleps sp., oviposited freely on Fraser fir. Some of the imported predators 
may have become established on other types of vegetation where their microclimatic and nutritional 
needs (i.e., suitable prey) were met. 


The established predators were considered ineffective, individually and as a group, in preventing tree 
mortality. Even in areas where the predators were well established, adelgid populations generally 
increased and trees continued to die. 


For all areas infested by the balsam woolly adelgid, tree killing has slowed, probably because most 
of the highly susceptible trees have been killed, and, in the case of Fraser fir in North Carolina, 
almost all overstory trees are dead. As the next generation of fir grows to maturity, the most 
susceptible trees may be killed by the balsam woolly adelgid, but it is expected that selection will 
occur for trees that are more tolerant of the adelgid. Predators are likely to play a greater role in 
prolonging the lives of scattered, semitolerant trees of the next generation than occurred when 
thousands of highly susceptible trees were infested during the first exposure to the adelgid. With time 
and selection of tolerant trees, the relationship between the adelgid and its hosts is expected to 
emulate that found in Europe and observed in a silver fir plantation in North Carolina where the 
adelgid causes little or no damage (Amman and Fedde 1971; Franz 1958). 


2. "Cypress aphid", Cinara cupressi (Buckton). By Mary Ellen Dix 


In 1990, Forest Pest Management (Forest Health), International Forestry's Tropical Forestry Program, 
the International Institute of Biological Control (IIBC) in Great Britain, the World Bank, United 


454 

















Nations Development Program (UNDP), and the United Nations Food and Agricultural Organization 
(FAO) initiated a cooperative project with Kenya's Forestry Department to identify potential 
parasites and predators of Cinara cupressi, an aphid from Central America that is a pest of tropical 
cypress in East Africa. In 1986, this aphid was discovered in Malawi. By 1991, the aphid had spread 
to Kenya and was severely damaging cypress, an important timber producing tree. 


Dan Kucera (Northeastern Area, State and Private Forestry), was assigned to coordinate Forest 
Service participation in the project. In 1992, Denny Ward (Southern Region R-8, Asheville, NC) 
began a two-year detail to FAO in Kenya to deal with the emergency situation, initiate and monitor a 
research program, transfer research technology, and assist in the development of a forest pest 
management program in the Kenya Forestry Department. At the same time, Forest Service 
entomologists in the Rocky Mountain, Southwestern, Pacific Southwest, and Southern Regions, and 
the Northeastern Area of State and Private Forestry, searched for parasites and predators of C. 
subinae, a related pest of juniper in Colorado, Arizona, California, North and South Carolina, 
Virginia, Pennsylvania, and the New England states. They shipped live immatures of these natural 
enemies to IIBC in England for initial biological screening and host preference evaluation. Presently, 
the Forest Service, FAO, Canada, and IIBC are assisting the Kenya Forestry Research Institute 
develop facilities for mass rearing the natural enemies. 


3. Scales and mealybugs of pines. By Mary Ellen Dix 


During the 1980s, pyrethroid insecticides replaced organophosphates as the preferred aerially- or 
ground-applied insecticides for control of seed and cone insects. In 1982-83, Stephen Clarke and 
Gary DeBarr (Southeastern Forest Experiment Station, Athens, GA), in cooperation with C. Wayne 
Berisford (University of Georgia, Athens) identified parasites and predators of "striped pine scale”, 
Toumegella pini and "loblolly pine mealybug", Oracella acuta in Georgia loblolly pine seed 
orchards, and evaluated the impact of two commonly used pyrethroid insecticides on their 
abundance. Parasitism of T. pini was highest on unsprayed trees after the third insecticide 
application. Predation of female 7. pini was lowest on trees treated with azinphosmethyl. They 
concluded that aerial insecticide application in seed orchards had little effect on settling female scale 
insects, but can result in lower resident natural enemy populations (Clarke et al. 1989, 1990). 


Ill. BIOLOGICAL CONTROL OF FOREST PATHOGENS 


A. Forest Diseases. By Ned B. Klopfenstein, E.G. Kuhlman, Carol M. Schumann, and Mary Ellen 
Dix 


The USDA Forest Service has traditionally played a significant role in research to understand and 
develop biological controls for tree diseases. This area of Forest Service research has been reviewed 
recently (Stewart 1989). Initial studies are aimed at identifying and characterizing potential 
biological control agents, including antagonists, parasites, competitors, and predators of tree 
pathogens. It is generally believed that the vast majority of biological control agents are yet to be 
identified, and thus continued efforts to identify such agents are warranted. After identification, 
additional studies are needed to evaluate the range of activity and develop methods for effective 
application and maintenance of biological control agents. Continued studies also contribute to a 
better understanding of the complex interactions among host tree, pathogens, biological control 
organisms, and other biotic and abiotic components of a forest ecosystem. 


Since mycorrhizal interactions and wood-rotting organisms are covered elsewhere, other Forest 


Service research in biological control of tree diseases can be divided into three general categories of 
disease which follow. 


455 


1. Biological control of root and butt rots 


Organisms that are competitive, antagonistic, parasitic, or predatory to rhizosphere and 
wood-inhabiting fungi offer potential for biological control of root and butt rots. However, the 
complex dynamics of such organismal interactions can pose significant difficulties in deploying such 
biological control (Shaw and Roth 1978, 1980; Shaw and Kile 1991). Several studies have 
investigated the interactions of Trichoderma spp., fungal antagonists, with Phellinus weirti or 
Armillaria spp., the causal agents of root rots (Nelson and Thies 1984, 1985, 1986; Goldfarb et al. 
1985, 1989a and b; Nelson et al. 1987, 1988; Reaves et al. 1990). Virus-like particles in isolates of 
Armillaria sp. have been observed (Reaves et al. 1987, 1988), and may have potential for controlling 
these pathogens. In addition, mycophagous nematodes have shown potential for controlling 
Armillaria root rot (Riffle 1973). 


The principles of and potential for biological control of forest nursery diseases have been recently 
reviewed (James et al. 1993). Biological control of root disease caused by Rhizoctonia sp. and 
Pythium sp. has been investigated (Burdsall et al. 1980). In addition, studies were initiated at the 
North Central Forest Experiment Station (NCFES) laboratory in St. Paul, MN, to evaluate seed 
treatments with antagonistic and other beneficial organisms to control damping off and root rot of red 
pine and white pine caused by Fusarium spp. (C. Ocamb, personal communication, NCFES, 1993). 
Methods to assay soil for antagonistic fungi also have been developed (Li et al. 1969). 


2. Biological control of stem cankers and other stem diseases 


E.G. Kuhlman (Southeastern Forest Experiment Station [SE], Research Triangle Park, NC) studied 
the utility of hypovirulence in Cryphonectria parasitica for controlling chestnut blight disease on 
American chestnut during 1977-89. Hypovirulence apparently is caused by double stranded 
ribonucleic acid (dsRNA), which normally is a component of mycoviruses. Hypovirulence reduces 
the vigor or virulence of the fungus so that the tree resists infection and develops callus tissue rather 
than cankers. Kuhlman (1979, 1981b and c) verified that hypovirulent isolates can limit the spread of 
virulent isolates within young cankers. Conidia from hypovirulent isolates also limited spread of 
young cankers. A mix of conidia from four to 11 hypovirulent isolates converted 95% of a random 
selection of 98 virulent isolates from the eastern U.S. to the hypovirulent condition in culture 
(Kuhlman 1982, 1983; Kuhlman and Bhattacharyya 1984; Kuhlman et al. 1984). However, treatment 
with a conidial suspension from eleven hypovirulent isolates failed to enhance the survival of 
American chestnuts in a West Virginia field test. Apparently the endemic inoculum level and/or the 
diversity of virulent isolates was too great for the hypovirulent inoculum to overcome. Other studies 
also have investigated the ability of hypovirulent isolates to control the establishment of virulent 
cankers (Double 1982). As of 1993, Forest Service researchers in Delaware, OH, were attempting 
therapy for chestnut blight using Pseudomonas spp. 


During 1973-80, Kuhlman conducted a study of hyperparasitic microbes associated with Cronartium 
quercuum f. sp. fusiforme to determine their potential as biological control agents for fusiform rust 
disease. The hyperparasite Scytalidium uredinicola was discovered and described (Kuhlman et al. 
1976); it was quite effective at reducing aeciospore numbers in some areas of a gall, although its 
effect was limited to one year on any localized area (Kuhlman 1981a). Other workers have 
investigated potential biological control and interactions of Cronartium rusts with hyperparasitic 
fungi such as Tuberculina spp. (Mielke 1933; Hubert 1935a and b; Wicker 1970, 1980, 1981; Wicker 
and Wells 1968, 1970). Tuberculina maxima demonstrated a long-term effect on aecial sporulation, 
but its occurrence was limited to more northerly areas where rust incidence was lowest (Kuhlman 
and Miller 1976). Sphaerellopsis filum (as Darluca filum) reduced the production of basidiospores 
by C. q. fusiforme on oak, but the effectiveness of this hyperparasite for controlling fusiform rust 


456 


disease is limited by the short duration of the rust life cycle that occurs on oak leaves (Kuhlman and 
Matthews 1976; Kuhlman et al. 1978). 


Other FS research on the biological control of stem diseases includes evaluation of Arthrobacter sp. 
and Fusarium sp. as potential biological controls of pitch canker on Virginia and slash pines at the 
SE laboratory at Athens, GA (Barrows-Broaddus and Dwinell 1987a and b), and of suppressive 
strains of Streptomyces for control of the poplar leaf spot and canker pathogen Septoria musiva 
(=Mycosphaerella populorum) at the NCFES laboratory at St. Paul, MN (Ostry and Anderson, 1992). 


3. Biological control of vascular wilts 


Studies conducted by the FS on the biological control of vascular wilts have been ongoing since 
Shigo (1958) initiated a search for potential biological control agents associated with trees infected 
with Ceratocystis fagacearum. Subsequent studies have focused on the colonization of oak trees by 
endophytic Bacillus spp. and Pseudomonas spp. as potential controls for oak wilt (Brooks et al., 
1988a and b; Brooks 1989; Gehring 1990; Gehring et al. 1990). 


Additional research on control of oak wilt was begun at the FS laboratory in St. Paul, MN, 
investigating the colonization of oak trees with alternative Ophiostoma sp. to suppress sporulation 
and overland transmission of oak wilt pathogens (J. Juzwick, NCFES, St. Paul, MN, personal 
communication, 1993). Streptomyces spp. also have been assessed for their ability to control Dutch 
elm disease (O'Brien et al. 1984). Additionally, Forest Service researchers at Delaware, OH, initiated 
a program to identify bacterial and fungal endophytes of American elm that are antagonistic to the 
Dutch elm disease pathogen, Ophiostoma sp. Schreiber et al. (1988) isolated Bacillus subtilis FS94 
from American elm xylem which produced novel antibiotics in vitro (Chang and Eshita 1988), but 
the isolate failed to protect elms in subsequent studies. Eshita and Roberto (1991) isolated a 
nonfluorescent Pseudomonas gladioli, LC,, from American elm. This bacterium exhibited both 
antagonism and antibiosis in vitro, but failed to protect elms in greenhouse trials. The interaction of 
xylem-colonizing Bacillus spp. with Verticillium wilt of maples has also been investigated (Hall et 
al. 1986). 


4. Role of host tree resistance to diseases in biological control 


Although not classically considered a form of biological control, the genetic constitution of host trees 
can have an important impact on the incidence of disease and the effectiveness of other forms of 
biological control. Identification of disease-resistant seed sources and development of improved 
populations through selection and breeding have been important outcomes of Forest Service tree 
improvement programs. Reviewing those activities is beyond the scope of this historical perspective, 
but it is important to consider possible mechanisms of genetic resistance in any discussion of 
biological control. For example, partial resistance to pathogens conferred by elevated levels of 
phytoalexins might also confer "resistance" to hypovirulent strains, non-pathogenic epiphytes, or 
symbionts. Similarly, resistance conferred by introducing a gene with antimicrobial activity (such as 
chitinases, gluconases, or cecropins) can be expected to have an impact on microflora associated with 
that host. Alternatively, more specific types of resistance can be engineered that affect only the target 
pest (e.g., coat-protein mediated viral resistance). 


Modifying host resistance through genetic manipulation can be an important tool in designing and 
improving the effectiveness of biological controls. However, the underlying mechanism of resistance 
must be considered in the context of the control system into which it is being integrated. Because 
host resistance is such an important interacting factor with other forms of biological control, 
successful management and stabilization of pathogen populations will likely involve compatible 
combinations of biological control strategies that include host resistance. 


457 


5. Future trends in biological control research 


Because of current environmental, economic, and societal concerns with pesticide use, it seems likely 
that biological control will play a more prominent role in future management of tree diseases. 
Research will likely continue to identify biological control agents, evaluate application methods, and 
monitor ecological interactions. Rapidly developing techniques in molecular biology offer promise in 
the identification and characterization of biological control agents. In addition, molecular technology 
will allow the genetic engineering of biological control agents and the transfer of anti-pathogen genes 
from biological control agents to host trees. However, the ecological ramifications of genetic 
engineering for biological control will have to be thoroughly evaluated before considering 
deployment. 


Forest Service research has demonstrated the enormous potential to develop successful biological 
control strategies for woody plant diseases. Considerable biological control research has been 
initiated on root and butt rots, stem cankers and vascular wilts. Nevertheless, it seems likely that the 
vast majority of potential biological control agents and other interacting factors remain unidentified. 
Research is noticeably lacking on diseases caused by viruses, mycoplasma-like organisms, bacteria, 
and nematodes. Successful development and deployment of new biological control strategies is 
dependent on the continuation of long-term ecological studies that determine the interaction of 
biological control agents with the host tree, pathogens, beneficial organisms, and other components 
of the forest ecosystem. 


B. Mycorrhizal Symbiosis. By Randy Molina 


The word mycorrhiza literally translates as "fungus root" and defines the common association of 
specialized soil fungi with the fine, feeder roots of plants. Mycorrhizal associations represent one of 
the more widespread forms of mutualistic symbioses in terrestrial ecosystems. Indeed, the 
plant-fungus associates have co-evolved over the millennia such that each partner depends upon the 
other for survival. 


The mycorrhizal fungus basically serves as an extension of the plant root system, exploring soil far 
beyond the roots' reach and transporting water and nutrients to the roots. The uptake of phosphorus is 
an especially important function of mycorrhizae, and many plants depend upon the fungi to supply 
adequate quantities of phosphorus for healthy growth. Other plant benefits include protection of fine 
roots against pathogens; increased root length and branching that enhances nutrient absorption; 
increased root longevity; tolerance to drought stress; detoxification of soil toxins; and resistance to 
heavy metals. In return, the mycorrhizal fungi receive their primary energy from the plant in the form 
of simple sugars produced during photosynthesis and transported to the roots. 


Mycorrhizal fungi not only benefit host plants. They are also key soil organisms that participate in 
nutrient cycling and building of soil structure. Their great mycelial biomass in the soil and 
reproductive structures (mushrooms and truffles) are cornerstones in the complex food webs of 
terrestrial ecosystems. 


The importance of mycorrhizae to the productivity of trees and forest ecosystems was recognized 
early by the Forest Service. Indeed, Forest Service scientists have been pioneers and leaders in 
mycorrhiza research, publishing over 500 papers on mycorrhizae during the last 30 years. These 
efforts include breakthrough discoveries on the isolation and manipulation of mycorrhizal fungi; the 
development and application of procedures to inoculate tree seedlings with selected beneficial fungi 
to improve growth in the nursery as well as survival after outplanting; the taxonomic classification of 
major groups of mycorrhizal fungi; the ecological and physiological diversity of mycorrhizal fungi; 
and the functional biodiversity of mycorrhizal fungi in forest ecosystems. 


458 


Detailing the breadth of discoveries made by Forest Service scientists in mycorrhiza research is 
beyond the scope of this paper. What follows are historical and regional perspectives on the major 
thrusts and impacts by key personnel and laboratories. Selected references are provided to lead 
readers to the wealth of published information. 


Pioneering research. USDA research on mycorrhizae began with an extensive report by McArdle 
(1932) on the relation of mycorrhizae to conifer seedlings. Through field observations and laboratory 
and greenhouse experiments, McArdle provided new evidence on the ubiquitous occurrence and 
beneficial aspects of mycorrhizae to conifer seedlings. 


Mycorrhiza research by E. Hacskaylo and colleagues at the Forest Physiology Laboratory, Beltsville, 
MD, in the 1950s mark the true pioneering studies and leadership by the Forest Service. Hacskaylo 
studied with the grandfather of mycorrhiza research, Elias Melin, in Uppsala, Sweden, and returned 
with modern techniques to study the physiology of mycorrhizal fungi in the U.S. Hacskaylo and 
colleagues published extensively on the physiology of ectomycorrhizal fungi, including response of 
fungi to temperature, light, moisture stress, and pH, and developed techniques for synthesizing dual 
plant-fungus cultures still in use today (Hacskaylo 1953; Hacskaylo and Palmer 1955; Hacskaylo et 
al. 1965). Hacskaylo is considered a world authority on the physiology of ectomycorrhizal fungi and 
his early review on the carbohydrate physiology of mycorrhizae is a landmark reference (Hacskaylo 
1973). 


Hacskaylo was also very active on the international forestry scene and organized several international 
workshops through the International Union of Forestry Research Organizations (IUFRO). He 
conducted pioneering experiments on mycorrhizal inoculation of pine seedlings destined for sites 
where pines did not normally exist. For example, he established pines in Puerto Rico by inoculating 
them with mycorrhizal fungi from native pine stands in the U.S. (Vozzo and Hacskaylo 1971). His 
applied efforts in Puerto Rico set the stage for large-scale mycorrhizal inoculations around the world. 


Forestry Sciences Laboratory, Athens, GA. The work at Athens began with C. Bryan and B. Zak who 
identified, isolated and studied many ectomycorrhizal fungi of southern pines (Bryan and Zak 1961; 
Zak and Bryan 1963). Thus began a long history of FS leadership in the characterization of 
ectomycorrhizae and development of fungus culture collections for use by researchers worldwide. 
Zak (1964) also developed novel concepts and hypotheses on the role of mycorrhizal fungi in 
protecting roots against root pathogens. This line of investigation was taken up by D. Marx, who 
experimentally demonstrated the disease protecting attributes of several ectomycorrhizal fungi. For 
example, he found Leucopaxillus cerealis produced antibiotics antagonistic to fungal pathogens in 
the genera Cylindrocladium, Phytophthora, Polyporus, Poria (=Antrodia), Pythium, Rhizoctonia, and 
Sclerotium (Marx 1972, 1973). Marx (1972, 1973) later synthesized all information on this subject; 
these reviews became the basis for current research on the disease protection aspects of mycorrhizal 
fungi. 


In the early 1970s, Marx and colleagues began intensive research to develop practical application 
schemes for inoculating nursery seedlings with selected, beneficial mycorrhizal fungi. Their efforts 
brought worldwide attention to mycorrhiza research in forestry and paved the way for modern 
approaches in application of basic mycorrhiza research (Marx 1975, 1980; Marx et al. 1984). 


The mycorrhiza research program in Athens centered around the ectomycorrhizal fungus Pisolithus 
tinctorius (Pt). Pt is a common pioneering mycorrhizal fungus on trees in mine spoils. Recognizing 
that the extremely high soil temperature reported on mine spoils might limit fungal symbionts to a 
few adapted species, Marx et al. (1970) explored the temperature-growth interactions of Pt. They 
found that Pt formed more ectomycorrhizae with Pinus taeda seedlings at 34° C than at lower 
temperatures, and that mycelial cultures grew at temperatures as high as 40° C. Marx and Bryan 


459 


(1971) found that aseptically grown Pinus taeda seedlings colonized with Pt survived and grew as 
well at 40° C as at 24° C; by comparison, nonmycorrhizal seedlings or those colonized with the 
fungal symbiont Thelephora terrestris had lower survival and no growth at 40° C. Clearly, the heat 
tolerance was a major factor in allowing Pt to invade coal spoils. Marx and coworkers then surveyed 
strip-mined lands for the presence of Pt, and found it to be the dominant and often only 
ectomycorrhizal fungus of pine roots growing on coal wastes in Indiana, Pennsylvania, Ohio, West 
Virginia, Virginia, Kentucky, Tennessee, and Alabama, and on kaolin spoils in Georgia (Marx 1975). 


These findings prompted extensive investigation of ways to inoculate and establish Pt 
ectomycorrhizae on roots of pine seedlings for outplanting on mine spoils. Marx and Bryan (1975) 
developed techniques for preparing pure culture inoculum and inoculating nursery soil with Pt. They 
reported excellent success in establishing Pt in nurseries with doubled growth of inoculated seedlings 
over noninoculated controls (Marx et al. 1976). Inoculation with Pt basidiospores also succeeded. 
Most importantly, Pt inoculation significantly increased survival and growth of seedlings on mine 
spoils (Marx and Artman 1979), even on sites with a history of repeated failures of pine plantations. 
Pt inoculation also increased survival and growth of southern pines on routine reforestation sites 
(Marx et al. 1977), and the improved growth is evident today. 


The work with Pt culminated with the development of commercial procedures for the production of 
Pt inoculum and testing of this biological product nationwide. Approximately eight million seedlings 
were inoculated annually (as of 1993) in the southern U.S., using Pt from a commercial source. 


The often spectacular results of the Pt mycorrhiza research program at Athens and extensive efforts 
by Marx and colleagues to communicate their findings brought intense interest to mycorrhiza 
sciences worldwide. Marx traveled regularly to developing countries, promoting and initiating 
practical mycorrhiza research programs. His exhaustive efforts in promoting mycorrhiza research in 
international forestry programs was recognized in 1991 when he was awarded the Marcus 
Wallenberg Prize in Sweden. 


Another group at Athens, under the leadership of P. Kormanik, developed practical application 
schemes for inoculating hardwood trees such as sweetgum with vesicular-arbuscular mycorrhizal 
fungi. Kormanik et al. (1977, 1981, 1982) also contributed new discoveries on the genetic 
interactions of mycorrhizal fungi and tree hosts. 


Mycorrhiza research continues today in Athens within a newly developed Center for Tree Root 
Biology. Global climate change impacts on belowground ecology, belowground carbon allocation, 
and microbial interactions in the rhizosphere are current areas of emphasis. 


Forestry Sciences Laboratory, Corvallis, OR. Mycorrhiza research at Corvallis has focused on the 
ecology of mycorrhizal fungi found in the diverse forest habitats of the Pacific Northwest. During the 
1950s, E. Wright studied and described various types of ectomycorrhizae found on Douglas-fir and 
pine species in both nursery and field settings (Wright 1963). He also examined the impacts of forest 
disturbance on seedling mycorrhizal development. His field investigations provided early warning 
signs of the fragile nature of the belowground ecosystem (Wright and Tarrant 1958). Research efforts 
25 years later would confirm his early observations and expand the understanding of disturbance 
effects on soil fungus populations. 


A center of mycorrhiza expertise developed at Corvallis during the 1960s and 1970s under the 
leadership of J. Trappe. In a landmark publication, Trappe (1962) developed a host-fungus index for 
all known or suspected ectomycorrhizal associations in the world. This work continues to be a 
significant database for modern research on the biodiversity of ectomycorrhizal fungi. Trappe, and 
later B. Zak who arrived from the Athens laboratory, isolated ectomycorrhizal fungi and confirmed 


460 








their host ranges through pure culture mycorrhizal syntheses. Zak (1973) developed a modern 
classification scheme for ectomycorrhizae that has served as a basis for modern approaches to 
characterize and identify ectomycorrhizae on wild plants. During the 1970s and 1980s, R. Molina, J. 
Trappe, and others conducted extensive ectomycorrhizal fungus isolation work and pure culture 
syntheses to document the degree of host specificity found in ectomycorrhizal associations in the 
Pacific Northwest (Molina and Trappe 1982). They found that many ectomycorrhizal fungi are 
restricted to certain host genera or families while others have broader host ranges. Their work set the 
stage for modern studies on host-fungus recognition and patterns of host-fungus co-evolution 
(Molina et al. 1993). Their ectomycorrhizal fungus culture collection is one of the largest in the 
world and their isolates have been used in mycorrhiza research programs worldwide. 


Trappe's expertise on the taxonomy of mycorrhizal fungi provided a solid mycological foundation for 
later studies on mycorrhiza ecology. Trappe published numerous treatises on the taxonomy of 
ectomycorrhizal fungi, particularly the hypogeous (subterranean) fungi called truffles. In 1974, 
Gerdemann and Trappe published a landmark monograph on the Endogonaceae of the Pacific 
Northwest. The Endogonaceae includes all fungi that form vesicular-arbuscular mycorrhizae; the 
most common type of mycorrhizae in terrestrial ecosystems, this occurs on nearly all important crop 
plants. The great explosion of world research on vesicular-arbuscular mycorrhizae during the 1970s 
and 1980s can be attributed partly to this publication because it provided the first classification 
scheme for these widespread, critically important, yet difficult to identify fungi. The taxonomic 
expertise on mycorrhizal fungi at Corvallis attracted many visiting scientists to Corvallis for training 
and cooperative research. Trappe co-authored taxonomic descriptions of mycorrhizal fungi from 
habitats around the world (Trappe 1979, 1982). This tradition continues today through extensive 
mycological cooperation with scientists in Australia, Great Britain, Spain, Canada, Argentina, 
Mexico, Sweden, and several other countries. 


The Corvallis team also conducted research on practical applications of mycorrhiza. Trappe (1977) 
published a review and conceptual paper on the selection of mycorrhizal fungi for use in forestry; 
many of his concepts remain the basis for selecting beneficial fungi for seedling inoculation. Molina 
and Trappe followed leads by Marx and colleagues in Athens to develop fungus inoculum and 
inoculation procedures for Pacific Northwest hosts and fungi. Molina and others published 
extensively on the mycorrhizal fungus Laccaria laccata, and their isolates have been successful in 
improving performance of introduced Douglas-fir plantations in Europe (e.g., Molina 1982). In the 
1980s, M. Castellano joined the team and began an active mycorrhizal inoculation program using 
basidiospores of truffle fungi in the genus Rhizopogon. His efforts have proven the most successful 
in the Pacific Northwest and approximately 14 million seedlings are inoculated annually. He found 
that inoculation can improve seedling productivity in the nursery by reducing the number of cull 
seedlings, and improve outplanting survival on severely disturbed sites. Castellano and Molina 
(1989) published a section of an USDA Handbook that details modern methods of mycorrhizal 
inoculation in container nurseries. 


Reforestation failures in stressed, cut-over sites in southwestern Oregon and northern California 
provided impetus not only for seedling inoculation research, but also for studying disturbance effects 
on populations of mycorrhizal fungi. Using techniques similar to those pioneered by Wright, 
Corvallis scientists documented the effects of burning and organic matter depletion on fungus 
populations. M. Amaranthus demonstrated the positive effects of non-commercially valuable 
understory trees and shrubs on the maintenance of viable fungus populations following disturbance 
(Amaranthus and Perry 1989). From these studies, concepts of guild formation by hosts capable of 
forming mycorrhizae with compatible fungi have been developed (Perry et al. 1987; Molina et al. 
1993); the contribution of mycorrhizal fungi in the dynamics of forest succession have also been 
documented (Molina and Amaranthus 1991). Amaranthus now (1990) leads a team of scientists from 


46] 


various disciplines in a 200-year-long regional study on long-term ecosystem productivity, wherein 
the belowground ecosystem will be thoroughly integrated into the above ground ecology. 


Long before biodiversity became the buzzword it is today, mycorrhiza research at Corvallis 
recognized the need to explore the physiological and ecological diversity of mycorrhizal fungi. I. Ho 
published a series of papers on ecotypic variation of mycorrhizal fungi based on hormone and 
enzyme production (Ho and Trappe 1987). Application efforts emphasized the use of isolates adapted 
to diverse planting sites. Ecological research also emphasized the role of mycorrhizal fungi as 
belowground linkages in the complex forest foodweb. For example, Trappe and wildlife biologist C. 
Maser discovered the widespread phenomenon of mycophagy (fungus consumption) among forest 
mammals (Maser et al. 1978). Many small mammals eat the sporocarps of mycorrhizal fungi, 
especially truffle fungi; and the truffle fungi depend upon these mammals for spore dispersal. The 
relevance of mycorrhizal fungus sporocarps and mammal mycophagy in forest ecosystems becomes 
evident when one considers food chain linkages between trees, fungi, mammals and predators such as 
the endangered northern spotted owl. 


As part of a regional effort to document biological diversity in Pacific Northwest forest ecosystems, 
the mycorrhiza research team at Corvallis is currently focusing on landscape level studies of fungus 
populations. For example, J. Smith is conducting studies on the ectomycorrhizal fungus community 
structure in various age classes of Douglas-fir forests. Research has been conducted on the ecology 
and productivity of commercially harvested, edible forest mushrooms (sporocarps of ectomycorrhizal 
fungi) (Molina et al. 1993). Commercial harvest of these special forest products provides millions of 
dollars to the Pacific Northwest economy. A primary goal of the Corvallis mycology team is to 
develop knowledge and tools to integrate the biology and function of belowground microbes into 
holistic ecosystem management schemes. 


Forestry Sciences Laboratory, Moscow, ID. Mycorrhiza research in the northern Rocky Mountains 
has emphasized the influence of soil factors and harvest disturbance on natural ectomycorrhizal 
development on Douglas-fir, larch, and pine trees. The team of A. Harvey, M. Jurgensen, M. Larson 
(originally with USDA Forest Products Laboratory, Madison WI) and others have conducted 
numerous field studies on the seasonal distribution of ectomycorrhizae in natural forest communities 
(Harvey et al., 1978, 1980a and b, 1981, 1987). They found that ectomycorrhizal development was 
strongly related to organic matter content. A critical discovery was that the vast majority of 
ectomycorrhizae often occurred in buried wood, particularly on dry sites and during the driest times 
of the year. Their efforts clearly showed the importance of organic matter and wood in the 
functioning and maintenance of ectomycorrhizae, and thus the health of forest ecosystems. They also 
documented the effects of various disturbances to soil organic matter and subsequent effects on 
mycorrhizal development and tree vigor. They developed guidelines for maintenance of woody 
residue on harvested sites with the goal of maintaining the long-term productivity of the soil. Their 
research on interactions of mycorrhizal fungus populations with soil organic matter are regularly 
cited as pioneering efforts in forest soil biology. 


Forest Service mycorrhiza research elsewhere. J. Riffle conducted several studies on 

ectomycorrhizae of pines planted in Nebraska (Riffle 1972, 1989). He was noted for his work on the 
interactions of root nematodes with mycorrhizae. F. Ponder published several papers on 
vesicular-arbuscular mycorrhizae of white ash and black walnut in Illinois (e.g., Ponder 1984). 
Ponder also studied the influence of grasshoppers and rabbits on dissemination of mycorrhizal fungus 
propagules into coal spoils (Maser et al. 1978). 


The Forest Service has supported numerous cooperative studies of mycorrhizae with universities, 
private industry and other federal and state agencies. Forest Service scientists have also participated 
actively in university research programs around the country, sponsoring students, postdoctoral and 


462 


sabbatical fellows. They have organized many national and international meetings on mycorrhiza 
research. The leadership provided by Forest Service scientists and cooperators have advanced our 
understanding of the belowground ecosystem and provided management tools for maintaining forest 
productivity and healthy ecosystem functioning. 


C. Fungi Attacking Wood Products. By Terry L. Highley 


The potential of biological control to protect wood products against deterioration by microorganisms 
has been recognized for a long time, as indicated in a 1940 memorandum by Mae S. Chidester, Forest 
Products Laboratory (FPL), Madison, WI. In this memorandum, Chidester suggested that a better 
understanding of the combined effect of two or more wood-inhabiting fungi on wood would be 
beneficial in preventing or controlling the defects brought about by these organisms. She further 
suggested the possible use of Trichoderma lignorum (=viride) as a control for wood-decay fungi such 
as Lenzites sepiaria (=~Gloeophyllum sepiarium). Evidently this proposal was not followed with 
experimental work, or at least nothing was published, as no reference was found in the literature. 


The first published work by Forest Service scientists on the use of biological control of wood- 
attacking fungi appears to be that of Lindgren and Harvey (1952) at the FPL. In this work, they used 
fluoride pretreatment of southern pine pulpwood to enhance growth of Trichoderma. They observed 
reduced decay in the pulpwood treated with Trichoderma. But as recognized in a 1958 FPL problem 
analysis by R. Lindgren, and continuing to date, such biological control remains a young field 
requiring considerable exploratory work before any practical applications are developed. 


Verrall (1966) made preliminary incursions into the field of microorganism associations when he 
commonly observed the ubiquitous mold Trichoderma viride as the first colonizer on rain-wetted 
wood in the Southeastern States, and proposed that competition from molds might possibly be an 
additional factor restricting the number of decayers on exterior woodwork. The effect of two isolates 
of T. viride on 41 isolates of Gloeophyllum saepiarium, G. trabeum, and Daedalea berkeleyi 
(=Gloeophyllum mexicanum) were studied on malt agar and in soil-block tests (Verrall 1966). All 
three basidiomycetes on malt agar either grew compatibly with 7. viride or actually overgrew 
Trichoderma. Trichoderma did not prevent decay of pine by the basidiomycetes. In a number of 
cases, decay was greater in the presence of Trichoderma than in pure culture. These findings are 
important because the three basidiomycetes are the prevalent decayers of pine lumber on the exterior 
of buildings and of other pine products exposed off the ground but subject to rain wetting. 


Following these rudimentary observations, biological control of wood-attacking fungi in wood 
products did not gain further attention by Forest Service scientists until the 1980s. Renewed interest 
was prompted by increasing environmental concerns which stimulated search for less hazardous 
wood preservation technology by scientists at the FPL. 


Polyoxin D, one of a group of peptidyl pyrimidine antibiotics produced by Streptomyces cacaoi var. 
asoensis was studied by Johnson (1980, 1982, 1986; Johnson and Chen 1983) for control of wood- 
staining mold and decay fungi. This antibiotic is a highly specific inhibitor of the chitin-synthetase 
enzyme. Because chitin synthesis occurs only in lower life forms, its inhibition could be a target- 
specific approach to pest control with minimal effect on non-target organisms such as mammals, 
birds, etc. Wood decay by several white and brown rot fungi was reduced by a 10 ppm polyoxin 
mixture and prevented at 100-700 ppm, an appreciably lower threshold than that of 
pentachlorophenol. However, against mold and stain fungi, polyoxin was not so effective and is not a 
good candidate for protection of wood against these fungi (Johnson 1986). Although polyoxins are 
not themselves suitable wood preservatives, these studies have tentatively validated the concept of 
wood preservation via inhibition of fungal chitin synthesis. 


463 


Highley and Ricard (1988) studied the antagonistic ability of Gliocladium virens and various 
Trichoderma spp. against important white- and brown-rot fungi. Gliocladium virens and the 
Trichoderma spp. overgrew the decay fungi cultured on the malt-agar medium and in most cases 
killed them. In soil-block tests, pretreatment of southern pine blocks with G. virens prevented 
brown-rot decay but was ineffective against the white-rot fungi. Similarly, Trichoderma spp. 
generally prevented or reduced decay by the brown-rot fungi, except for Gloeophyllum trabeum, but 
also were generally ineffective against the white-rot fungi. Various concentrations of ammonium 
nitrate (NH,NO,) and glucose in a basal medium did not affect antagonism of Trichoderma spp. in 
wood blocks. Gliocladium virens did not confer residual fungistasis to wood blocks. In soil-block 
tests of wood blocks, G. virens arrested the growth of Antrodia carbonica, but not other decay fungi. 
This work suggests that Gliocladium and Trichoderma have potential as natural agents for biological 
control of wood decay. 


Several studies were conducted by scientists at the FPL assessing the potential and application of 
commercial Trichoderma preparations for control of wood decay fungi. These preparations are 
mainly available as a wettable powder and as pellets both containing propagules of Trichoderma 
spp.: ATCC 20475 (T-75) and 20476 (T-76) (American Type Culture Collection). Both are produced 
in Toreboda, Sweden, by Bio Innovation AB(BINAB™). Looking into the mode of action of T-75 
and T-76, Murmanis et al. (1988a and b) found that Trichoderma strains did not produce either water 
soluble antibiotics or exoenzymes in wood blocks but protected the wood against major brown-rot 
basidiomycetes. Abundant chlamydospore formation was observed. Murmanis et al. (1988b) showed, 
also on SEM microphotographs, that T-75 and T-76 spores became attached readily to hyphae of 
wood decay basidiomycetes. These spores germinated on the surface of the basidiomycete hyphae 
and broke through its wall. 


In another study on mode of action by Trichoderma (Bruce and Highley 1991a), the interactive 
effects of Trichoderma strains, including T75 and T76, against a range of wood decay fungi was 
examined with particular attention given to the production of soluble metabolites by the antagonists. 
It was obvious from the results of this study that the modes of antagonism of Trichoderma spp. are 
most complex and, unlike the mode of action of most chemicals, may change with varying 
environmental conditions. This point is important and must be carefully considered in evaluation of 
control systems, particularly during screening tests for potential control agents. 


To be a successful biological control agent against wood decay fungi in wood products, the 
antagonistic effect must last many years. The results of a study by Bruce and Highley (1989a, 1991b) 
showed that wood material removed from poles treated with a Trichoderma-based (T-75, T-76) 
biological control product can resist attack by active fungi seven years after first inoculated. This 
work suggests that the use of biological control using these Trichoderma species might well, with 
further research, be valuable as a prophylactic treatment to protect poles from internal decay. Most 
importantly the decay prevention observed in this experiment was achieved using material treated 
with Trichoderma under field conditions. This result indicates that at least some of the modes of 
antagonism attributed to this fungus during laboratory studies must still be active in the nutrient- 
limiting environment in wood pole interiors. 


Wood products, such as poles, are commonly precolonized by a resident microflora, and any control 
agent must be able to either displace or coexist with a variety of mold organisms. With this in mind, 
Bruce and Highley (1989b) examined the direct influence that prior colonization of wood by typical 
mold residents from creosoted poles has on the biological control abilities of Trichoderma (T-75, 
T-76) against Neolentinus lepideus. The results of this study indicated that Trichoderma can protect 
wood from decay by N. /epideus even when the blocks are colonized with mold organisms prior to 
being treated with Trichoderma. 


464 





Trichoderma species examined for antagonistic effect against decay fungi have been rather selective 
in their antagonism in that they have not been able to control decay by the brown-rot fungus 
Gloeophyllum trabeum, and most white-rot fungi. In a search for antagonistic fungi with broader 
antagonism toward wood decay fungi, Highley (1989a and b) evaluated the antagonistic abilities of 
Scytalidium lignicola against several white- and brown-rot fungi. Pretreatment of Douglas-fir and 
southern pine blocks with S. /ignicola prevented decay by all fungi. Blocks that were heated or 
treated with propylene oxide to kill the antagonist were not decay resistant. Thus, S. /ignicola does 
not confer a residual fungistatic effect to wood. Scytalidium lignicola was able to eradicate all the 
decay fungi in wood except for Postia placenta and Gloeophyllum trabeum. Wood blocks treated 
with sterilized filtrates of S. Jignicola were not decay resistant, and filtrates were not inhibitory to 
growth of the decay fungi in agar medium. The antagonistic effect, therefore, apparently does not 
involve toxins. 


The interspecific interactions and antagonism among several .Scytalidium isolates with various 
brown- and white-rot fungi was studied by Cease et.al. (1989). Scytalidium initially colonized the 
surface of the blocks and gradually overgrew the basidiomycetes. In individual wood blocks from 11 
Scytalidium-basidiomycete paired treatment combinations, the basidiomycete was inhibited only in 
some locations in the wood block. These wood blocks demonstrated interspecific interactions and 
antagonism between the different fungi. The white-rot fungi responded to isolates of Scytalidium by 
occluding xylem cells with masses of hyphae, forming pseudosclerotial plates in the zone of initial 
interaction. Scytalidium appeared to gain access into portions of wood colonized by the 
basidiomycetes only after substantial decay had resulted by the wood decay fungus. 


In several studies at the FPL, scientists examined the efficacy of bacteria as biological control agents 
against wood-decay fungi and sapwood-inhabiting fungi. The type of medium used in evaluation 
studies of bacterial-fungal interaction had considerable effect on interactions on agar and wood 
(Benko and Highley 1991a and b). In an initial decay test, a bacterial preparation prevented decay by 
a white- and brown-rot fungus when tested by an agar-block procedure (Benko and Highley 1990a). 
However, in further testing, using the soil-block method, the bacterial preparation was ineffective 
(Benko and Highley 1990b). Evidence that actively growing bacteria are needed for successful 
biological control by the bacterial treatment was provided by the failure of the autoclaved bacterial 
solution to protect wood from decay. This is discouraging from the standpoint of long-term 
protection against decay because there would probably be no residual fungistatic effect in the wood 
after death of the bacteria. 


Bacterial preparations were found to be very effective in preventing stain and mold discoloration of 
various wood species in laboratory tests (Benko and Highley 1990a, 1991b). The greatest potential 
for use of bacteria, therefore, may be for protection against mold and stain in green logs or lumber 
where only temporary protection is needed. 


An interesting observation was made by Croan and Highley (1991) who found that the blue stain 
fungus Ceratocystis coerulescens could be controlled by metabolic products released by several 


wood decay basidiomycetes. In this case, it might be possible to protect wood against discoloring 
fungi by treatment with fungitoxic metabolic products. 


IV. BIOLOGICAL CONTROL OF WEEDS 
A. Dwarf Mistletoes. By Ned B. Klopfenstein and Mary Ellen Dix 
The name "mistletoe" is often applied to the 2,000 species of parasitic plants belonging to the 


families Loranthaceae and Viscaceae. Dwarf mistletoes (Arceuthobium spp.) are the most abundant 
mistletoes and they are widely distributed and cause serious damage to high value timber trees (Gill 


465 


and Hawksworth 1961). Most research on the biological control of mistletoes has been directed 
toward cataloguing the native fungi and insect associates of mistletoe and learning about their 
biology (Gill and Hawksworth 1961; Wicker and Shaw 1962, 1968; Hawksworth 1972; Knutson 
1978: Knutson and Hutchins 1979). At least ten fungal pathogens of dwarf mistletoe have been 
identified on shoots or fruits. Three of these fungi, Septogloeum gillii, Colletotrichum 
gloeosporioides, and Wallrothriella arceuthobii, are common and widespread in North America. 
Wallrothriella arceuthobii occurs throughout much of Canada, the western U.S., and northern 
Mexico. It attacks only pistillate flowers of certain spring-flowering species and prevents maturation. 
Colletotrichum gloeosporioides occurs in the western U.S., and attacks the shoots and reduces the 
reproductive potential, while S. gillii causes shoot anthracnose in the western U.S. and Canada 
(Wicker 1967; Wicker and Shaw 1968; Hawksworth 1972). Although birds and mammals can also 
adversely affect mistletoe, there has been no attempt to catalogue these interactions. Results to date 
indicate that insects may be the most effective natural control of mistletoe (Hawksworth 1972). 


B. Hawaiian Forests and Plantings. By Mary Ellen Dix and George P. Markin 


Introduced plants have long been recognized as one of the major threats to the continued existence of 
unique island forest ecosystems in Hawaii. Approximately half of these plants were introduced by 
immigrants as fruit, flowers, and ornamentals. Most others were introduced as forage plants in an 
effort to improve pastures or trees for reforestation or forest improvement (Neal 1965; Smith 1985). 
Due to lack of natural enemies that were left behind in the original homeland, these weeds can 
outgrow, out reproduce, and outspread native flora of Hawaii. 


The Hawaiian forest weed program is a cooperative effort between five state and federal agencies: 
the Hawaii Department of Land and Natural Resources, USDI National Park Service, USDA Forest 
Service, Hawaii Department of Agriculture, and the University of Hawaii (Markin 1989). In 1982, 
the first foreign explorer involved in this program was sent to South America to hunt for natural 
enemies of Hawaii's most serious forest weed, banana poka (Gardner and Davis 1982; Markin, 1989, 
1991; Smith 1990; Markin and Yoshioka 1992; Markin et al. 1992a and b). In 1983, construction 
began on an insect quarantine facility in the Hawaii Volcanoes National Park on the island of Hawaii 
specifically devoted to biological control of forest weeds. The facility was completed in 1984 and 
certified by both the State of Hawaii and USDA-APHIS to contain insects for study in an escape- 
proof environment. The first shipment of insects arrived in 1985, and the release of the first 
biological control agent from this facility occurred in 1987 (Markin 1991). Because Hawaii is 
geographically isolated, the forest weed control program has utilized the State of Hawaii's procedures 
and protocols for introductions and releases of biological control agents, which differ somewhat from 
those for mainland U.S. 


Initially, all pathogen testing was conducted in the country of pathogen origin or in a converted germ- 
warfare facility operated by the ARS in Frederick, MD. In 1992, the first pathogen quarantine facility 
specifically designed and devoted to the biological control of weeds was opened in Honolulu by the 
Hawaii Department of Agriculture. Pathogens of forest weeds, firetree, and blackberry were the first 
studied in this facility (Markin 1993). 


By 1993, the forest weed program was targeting banana poka, gorse, "firetree", blackberry, 
"strawberry guava", and "Koster's curse". The first insect release was in 1987, only six years ago, but 
the natural enemy populations appear to be growing and feeding damage already is visible on two of 
the weed species: Koster's curse and gorse. To date, seven species of insects and one pathogen have 
been released; see summary of this work by Markin et al. (1992). Two species of insects and two 
species of pathogens were in quarantine undergoing final stages of evaluation as of 1993. Ten more 


species of natural enemies were in various stages of study within quarantine, and 20 more were being 
studied in foreign countries. 


466 











These programs, however, are far from complete. Most of the targeted weeds have only one or two 
agents established against them, primarily insects or pathogens that attack only the foliage. The task 
of introducing new natural controls for the few weeds already targeted (not to mention those not yet 
targeted) will require the release of additional insects and pathogens, and will take five to ten more 
years of research (Markin 1993) and another 20 or more years before biological control becomes 
effective. The present program has demonstrated that biological control of forest weeds is feasible 
and that the technology can be developed to implement it. Nevertheless, at least 20 additional weeds 
must be controlled within the next 20 to 50 years if Hawaiian forest communities are to survive 
(Smith 1989). 


V. AUTHOR LIST 


Gene D. Amman (retired), USDA Forest Service, Intermountain Forest and Range Experiment 
Station, 324 25th St., Ogden, UT 84401. 

Leah S. Bauer, USDA Forest Service, North Central Forest Experiment Station, Michigan State 
University, Stephen S. Nisbet Bldg., 1407 S. Harrison Rd., East Lansing, MI 48823. 

Karen M. Clancy, USDA Forest Service, Rocky Mountain Forest and Range Experiment Station, 
Southwest Forest Science Complex, Flagstaff, AZ 86001-6381. 

Mary Ellen Dix, USDA Forest Service, Rocky Mountain Forest and Range Experiment Station, 
National Agroforestry Center, University of Nebraska, Lincoln, NE 68583-0822. 

John H. Ghent, USDA Forest Service, Southern Region, Forest Pest Management, 200 Weaver 
Boulevard, Asheville, NC 28804. 

Terry L. Highley, USDA Forest Service, Forest Products Laboratory, One Gifford Pinchot Drive, 
Madison, WI 53705-2398. 

Shivanand Hiremath, USDA Forest Service, Northeastern Forest Experiment Station, Forestry 
Sciences Laboratory, 359 Main Road, Delaware, OH 43015. 

Donald N. Kinn, USDA Forest Service, Southeastern Forest Experiment Station, Alexandria Forestry 
Center, 2500 Shreveport Highway, Pineville, LA 71360. 

Ned B. Klopfenstein, USDA Forest Service, Rocky Mountain Forest and Range Experiment Station, 
National Agroforestry Center, University of Nebraska, Lincoln, NE 68583-08272. 

E.G. Kuhlman, USDA Forest Service, Southeastern Forest Experiment Station, 320 Green Street, 
Athens, GA 30602-2044. 

George P. Markin, USDA Forest Service, Pacific Southwest Forest and Range Experiment Station, 
Institute of Pacific Islands Forestry, 1151 Punchbowl Street, Honolulu, HI 96813. 

Mauro Martignoni (retired), USDA Forest Service, Rocky Mountain Forest and Range Experiment 
Station, Forestry Sciences Laboratory, 2205 Columbia, S.E., Albuquerque, NM 87106. 

Randy Molina, USDA Forest Service, Pacific Northwest Forest and Range Experiment Station, 3200 
SW Jefferson Way, Corvallis, OR 97331. 

Thomas M. ODell, USDA Forest Service, Northeastern Forest Experiment Station, Center for 
Biological Control of Northeastern Forest Insects and Diseases, 51 Mill Pond Road, Hamden, CT 
06514. 

John D. Podgwaite, USDA Forest Service, Northeastern Forest Experiment Station, Center for 
Biological Control of Northeastern, Forest Insects and Diseases, 51 Mill Pond Road, Hamden, 
CT 06514. 

Roger B. Ryan (retired), USDA Forest Service, Pacific Northwest Forest and Range Experiment 
Station, Forestry and Range Sciences Laboratory, 1401 Gekeler Lane, La Grande, OR 97850. 

Richard F. Schmitz (retired), USDA Forest Service, Intermountain Forest and Range Experiment 
Station, 324 25th Street, Ogden, UT 84401. 

Carol M. Schumann, USDA Forest Service, Rocky Mountain Forest and Range Experiment Station, 
National Agroforestry Center, University of Nebrask-a, Lincoln, NE 68583-0822. 


467 


James M. Slavicek, USDA Forest Service, Northeastern Forest Experiment Station, Forestry 
Sciences Laboratory, 359 Main Road, Delaware, OH 43015. 

Al Valaitis, USDA Forest Service, Northeastern Forest Experiment Station, Forestry Sciences 
Laboratory, 359 Main Road, Delaware, OH 43015 


VI. ACKNOWLEDGMENTS 


Special thanks are given to all who helped research and produce the 'Overview' (Chapter 5) and 
detailed 'History of Biological Control in the Forest Service’ (Appendix III) including: Frances 
Barney for her diligent efforts in obtaining obscure publications and information; Jennifer Irwin for 
her assistance in identifying, obtaining, and recording the cited publications; Jane Deger, LeAnne 
Gustafson, Marcia Gustafson, and Chris Hobson for their help in locating publications; and Sylvia 
Christensen, Eleanor Oler, Jennifer Lindgren, and Michael Barnhart for their assistance in typing 
parts of the manuscript. Technical reviews of sections or the entire manuscript were made by 
numerous people including Leah Bauer, Arnold Drooz, Normand Dubois, Lane Eskew, Gerard 
Hertel, Donald Kinn, Ned Klopfenstein, Daniel Jennings, Richard Mason, Thomas ODell, Katherine 
Parker, Richard Reardon, Carol Schumann, James Slavicek, and Torolf Torgersen. 


VI. REFERENCES 


Allen, D.C., F.B. Knight, J.L. Foltz, and W.J. Mattson. 1969. Influence of parasites on two 
populations of Choristoneura pinus (Lepidoptera: Tortricidae) in Michigan. Annals of the 
Entomological Society of America 62:1469-1475. 


Amaranthus, M.P., and D.A. Perry. 1989. Interaction effects of vegetation type and Pacific madrone 
soil inocula on survival, growth, and mycorrhiza formation of Douglas-fir. Canadian Journal of 
Forest Research 19:550-556. 


Amman, G.D. 1961. Predator introductions for control of the balsam woolly aphid on Mt. Mitchell, 
North Carolina. USDA Forest Service, Southeastern Forest Experiment Station, Research Note 153, 


2 pp. 


Amman, G.D. 1970. Prey consumption and variations in larval biology of Enoclerus sphegeus 
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52 


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534 


Table 1. Predators and parasites of the mountain pine beetle in lodgepole pine (DeLeon 1934b; 
Amman and Cole 1983) 


Order 


PHYLUM ARTHROPODA, CLASS INSECTA 


HETEROPTERA 


COLEOPTERA 


DIPTERA 


HYMENOPTERA 


Family 


Anthocoridae 
Cleridae 


Colydidae 
Cucujidae 


Histeridae 
Nitidulidae 


Pythidae 
Rhizophagidae 
Staphylinidae 


Tenebrionidae 
Trogossitidae 


Asilidae 
Dolichopodidae 
Lonchaeidae 
Xylophagidae 
Braconidae 
Eurytomidae 
Pteromalidae 


Species 


Several species 

Enoclerus lecontei (Wolcott) 

Enoclerus sphegeus (Fabricius) 

Thanasimus undatulus Say 

Lasconotus complex LeConte 

Cucujus clavipes Fabricius var. puniceus 
Mannerheim 

Isolomalus mancus Casey 

Platysoma punctigerum LeConte 

Epurea inearis Maklin 

Glischrochilus vittatus (Say) 

Pytho planus Herbst 

Rhizophagus procerus Casey 

Nudobius sp. 

Quedius longipennis Mannerheim 

Corticeus parallelus (Melsheimer) 

Corticeus substriatus (LeConte) 

Temnochila virescens (Fabricius) var. chlorodia 

Mannerheim 

Laphria gilva (Linnaeus) 

Medetera aldrichii Wheeler 

Lonchaea viridana Meigen 

Xylophagus abdominalis Loew 

Coeloides dendroctoni Cushman 

Eurytoma cleri Ashmead 

Dinotiscus acutus (Provancher) 

Dinotiscus burkei (Crawford) 

Dinotiscus dendroctoni (Ashmead) 

Rhopalicus pulchripennis (Crawford) 

Roptrocerus xylophagorum (Ratzeburg) 


Continued 


33.9 


Table 1. Predators and parasites of the mountain pine beetle in lodgepole pine (DeLeon 1934b; 
Amman and Cole 1983)--Continued 


Order 


PHYLUM NEMATA, CLASS SECERNENTIA 


APHELENCHIDA 


RHABDITIDA 


TYLENCHIDA 


Family 


Aphelenchidae 


Diplogasteridae 
Panagrolaimidae 


Sphaerulanidae 
Allantonematidae 


PHYLUM CHORDATA, CLASS AVES 


Caprimulgiformes 
Passeriformes 


Piciformes 


a ee ees 


536 


Caprimulgidae 
Certhiidae 
Corvidae 
Emberizidae 
Muscicapidae 


Paridae 
Sittidae 


Tyrannidae 


Picidae 


Species 


Bertsenus brachycephalus (Thorne) Massey 
Bursaphelenchus conurus (Steiner) Goodey 
Bursaphelenchus talonus (Thorne) Goodey 
Cryptaphelenchus latus (Thorne) Ruhm 
Ektaphelenchus tenuidens (Thorne) 
Parasitaphelenchus acroposthion (Steiner) Ruhm 
Mikoletzkya pinicola (Thorne) Baker 
Panagrolaimus dentatus (Thorne) Ruhm 


Sphaerulariopsis hastata (Khan) Nickle 
Contortylenchus reversus (Thorne) Ruhm 


prob. Chordeiles minor Forster 
Certhia americana Bonaparte 
Nucifraga columbiana (Wilson) 
Dendroica coronata (Linnaeus) 
Mydaestes townsendi Audubon 
Turdus migratorius Linnaeus 
prob. Sialia currucoides (Bechstein) 
Parus gambeli Ridgeway 

Sitta carolinensis Latham 

Sitta pygmaea Vigors 

prob. Sitta canadensis Linnaeus 
Contopus borealis Swainson 
Contopus sordidulus Sclater 
Empidonax sp. 

Picoides pubescens Linnaeus 
Picoides tridactylus Linnaeus 
Picoides villosus Linnaeus 


Table 2. Predator liberations against Adelges piceae (Ratzeburg) in Northeastern United States, 


1954-1959 


Species 


Coleoptera 
Coccinellidae 
Pullus impexus (Mulsant) 
Derodontidae 
Laricobius erichsonii Rosenhauer 


Diptera 
Chamaemyiidae 
Leucopis obscura Haliday 
Cecidomyiidae 
Aphidoletes thompsoni Moehn 


TOTAL 


Origin 


Europe 


Europe 


Europe 


Europe 


Where 
Liberated 


VT 

ME 
NH,VT 
NH,NY,VT 


ME 


Number 
Year Released 
1955 268 
1955 16,193 


959 


1954-56 3,744 


1959 1,185 


21S 90 


537 


Table 3. Predators liberated against Adelges piceae (Ratzeburg) in North Carolina, 1959-1966 








Number 
Species Origin Year Released 
Coleoptera 
Coccinellidae 
Aphidecta obliterata (L.) Germany/Austria 1960, 1966 Twa 802 
Pullus impexus (Mulsant) Germany 1960, 1966 11,606 
Scymnus pumilio (Weise) Australia 1960 3,300 
Adalia tetraspilota (Hope) Pakistan 1961 65 
Adonia variegata Goeze India 1961 15 
Ballia eucharis Mulsant India 1961 209 
Calvia sp. India 1961 35 
Harmonia breiti Mader India/Pakistan 1961 131 
Oenopia sauzeti Mulsant India 1961 90 
Derodontidae 
Laricobius erichsonii Rosenhauer Germany 1959-1962 14,006 
Diptera 
Chamaemyiidae 
Leucopis obscura Haliday New England 1960, 1962 1,508 
Leucopis prob. griseola (Fallén) Germany 1961 148 
Leucopis spp. (3 species) India 1962-1964 1,646 
Cecidomyiidae 
Aphidoletes thompsoni Moehn Germany Lo59 8,809 
Syrphidae 
Metasyrphus sp. Germany 1961 36 
Heteroptera 
Anthocoridae 
Tetraphleps (probably 2 species) India/Pakistan 1963-1965 782 
Neuroptera 
Chrysopidae 
Chrysopa (sens. lat.) (2 species)India 1961-1962 636 
Hemerobiidae 
Hemerobius sp. India 1961-1963 341 
TOTAL 46,325 


538 


Table 4. Predators liberated against Adelges piceae (Ratzeburg) in Oregon and Washington, 


1957-1965 


Species 


Coleoptera 
Coccinellidae 
Adalia luteopicta Mulsant 
A. tetraspilota (Hope) 
Aphidecta obliterata (L.) 


Ballia eucharis Mulsant 

Chilocorus kuwanae Silvestri 

Exochomus lituratus Gorham 

E. uropygialus Mulsant 

Harmonia breiti Mader 

Leis dimidiata (F.) 

Pullus impexus Mulsant 

Scymnus pumilio (Weise) 

Synharmonia conglobata (L.) 
Derodontidae 

Laricobius erichsonii Rosenhauer 


Diptera 
Chamaemyiidae 
Cremifania nigrocellulata Czerny 


Leucopis obscura Haliday 


Leucopis sp. 
Cecidomyiidae 
Aphidoletes thompsoni Moehn 


Neuroptera 
Chrysopidae 
Chrysopa (sens. lat.) sp. 


Heteroptera 
Anthocoridae 
Tetraphleps sp. 


TOTAL 


Origin 


India 
India 
Sweden/ 
Germany 
Pakistan 
Japan 
Pakistan 
Pakistan 
India 
India 
Germany 
Australia 
India 


Czechoslovakia/ 


Germany 


Czechoslovakia/ 


Germany 
Maine 


(ex Europe) 


Pakistan 


Czechoslovakia/ 


Germany 


India 


India/ 
Pakistan 


Where 
Liberated 


OR 
OR,WA 
OR 


OR 


OR 


OR,WA 


Year 


1960 
1959-60 
1958-63 
1959 
1958 
1960 
1959-60 
1959 
1959. 
1960-62 
1959-60 
159 


1958-62 


1958-59 
1958-59 
1930 


RPI, 


1961 


1964 


Number 
Released 


20 

89 
PAK | 
85 
135 
43 
4,741 
10 

23 
1,342 
2,859 
121 


12,406 


1,374 


2,785 


333359 


63 


98 


61,785 





a39 


2 es 3 


fat get a), Si se 


APPENDIX IV 


ABBREVIATIONS 
Compiled by S. M. Braxton 


. Australian Biological Control Laboratory (ARS) 


United States Army Corps of Engineers 


.. Autographa californica (cabbage looper) multiply-occluded nuclear polyhedrosis virus 


American foulbrood (Bacillus larvae) 


. Anagrapha falcifera (celery looper) multiply-occluded nuclear polyhedrosis virus 


Appalachian Fruit Research Station (ARS) 

U.S. Agency for International Development 

Appalachian Integrated Pest Management (FS, Forest Pest Management) 
APHIS Management Team 


. Air National Guard Base 


aminopeptidase-N 


. Animal and Plant Health Inspection Service (USDA) 


Asian Parasite Laboratory (BE and ARS) 
Agricultural Research and Education Service (USDA) 
Agricultural Research Service (USDA) 


. Collection of Entomopathogenic Fungal Cultures (ARS) 


American Society for Horticultural Science 


. American Type Culture Collection 


adenosine triphosphate 


.. Aquatic Weeds Research Laboratory, Fort Lauderdale, FL 
. Beltsville Agricultural Research Center (USDA) 
.. Binational Agricultural Research and Development Program 


Biological Assessment and Taxonomic Support (APHIS, PPQ) 
Biotechnology, Biologics and Environmental Protection (APHIS) 
Biosystematics and Beneficial Insects Institute (ARS) 


. Biological Control Coordinating Council (USDA) 
. Biological Control Documentation Center (ARS) 


Biological Control of Insects Laboratory (ARS) 


. Biological Control of Insects Research Laboratory (ARS) 


Biological Control Operations (APHIS, PPQ) 


. Biological Control of Weeds Research Laboratory, Albany, CA (ARS) 


Bureau of Entomology (USDA) 

Bureau of Entomology and Plant Quarantine (USDA) 
Beneficial Insect Introduction Laboratory (ARS) 
Beneficial Insects Introduction Research (ARS) 
Beneficial Insects Laboratory (ARS) 


.. Bio Innovation AB 


Beneficial Insects Research Laboratory (ARS) 
billion International Units 
Biocontrol of Plant Diseases Laboratory (ARS) 


1 Oe Bureau of Plant Industry (USDA) 
BPISAE ... Bureau of Plant Industry, Soils, & Agricultural Engineering (USDA) 
BD be ay 2 ss black turpentine beetle 


Sh © Seren Bacillus thuringiensis and Bacillus thuringiensis thuringiensis 

BRD Ok Bacillus thuringiensis israeliensis 

BtICP .... International Cooperative Program on the Spectrum of Activity of Bt 

CANUSA . Canada/United States Spruce Budworms Program 

CON ee Customer Advisory Panel 

EBC eo. classical biological control 

GES co. ks Cooperative Extension Service 

CFRP .... Combined Forest Pest Research and Development Program (USDA) 

OG A os: Colletotrichum gloeosporioides f. sp. aeschynomene 

GIBC:..... Commonwealth Institute of Biological Control (see also International Institute of 
Biological Control, IIBC) 

CIRAD ... Centre International de Recherche Appliqué et de Développement, France 

CEB eos aus cottonwood leaf beetle 

1S rr centimeter 


COSEPUP Committee on Science, Engineering, and Public Policy, National Academy of Sciences 
(O¢ ee Colorado potato beetle 


CPRU .... Cotton Pathology Research Unit (ARS) 

oA ee cytoplasmic polyhedrosis virus 

GRIS ..... Current Research Information System 

CSIRO ... Commonwealth Scientific and Industrial Research Organization, Australia 
CSREES .. Cooperative State Research, Education and Extension Service (USDA) 
CSRS ..... Cooperative State Research Service (USDA) 

118 i dichloro dipheny] trichloroethane 

DFTM .... Douglas-fir Tussock Moth 

DNA ois: deoxyribonucleic acid 

dsRNA .... double stranded ribonucleic acid 

EBCL .... European Biological Control Laboratory (ARS) 

ECB. +... European corn borer 

BOVs.. extracellular viruses 

MOB oc... ethylene dibromide 

11 OU rn European foulbrood 

Ve Pe ecdysteroid glucosyl transferase 

ELISA .... enzyme-linked immunosorbent assay 

EF 3.3. ectomycorrhizal fungi 

BOA. sss Environmental Protection Agency 

12 European Parasite Laboratory (BE and ARS) 

BRS: 2.3 ..:: Economic Research Service (USDA) 

iecs . ete Extension Service (USDA) 

ESCOP ... Experiment Station Committee on Organization and Policy 
ESPBRAP . Expanded Southern Pine Beetle Research and Applications Program (USDA) 
(0) Experimental Use Permit 

BAO Goes. Food and Agricultural Organization (United Nations) 

HAS i. Foreign Agricultural Service (USDA) 

FBCL .... Florida Biological Control Laboratory 

BRA: ss fetal bovine serum 

UAL ica ws Food and Drug Administration 

FIDM .... Forest Insect and Disease Management (FS) 

FIDR ..... Forest Insect and Disease Research (FS) 


541 


IPI 


se 8 we 


oe eee 


. Federal Insecticide, Fungicide, and Rodenticide Act 


Division of Forest Insect Research (FS) 
few polyhedra (mutant strain of LdNPV) 
Forest Products Laboratory (FS) 

Forest Pest Management (FS) 

Forest Service (USDA) 


. Gulf Coast Mosquito Research Laboratory, Lake Charles, LA (ARS) 
. Grasshopper Integrated Pest Management Project 


gypsy moth 


.. Gypsy Moth Life System Model 
. Gypsy Moth Research and Development Program (FS) 


glucouronidase 
granulosis virus 
human immunodeficiency virus 


. high performance liquid chromatography 
. Heliothis zea (corn earworm) singly-embedded nuclear polyhedrosis virus 


International Activities Office (ARS) 

Inter-agency Advisory and Action Team (USDA) 

institutional biosafety committee 

Interagency Biological Control Coordinating Committee (USDA) 
Insect Biocontrol Laboratory (ARS) 

insecticidal crystal protein 


. Insect Enemies of Aquatic Weeds Laboratory, Gainesville, FL (ARS) 


isoelectric focusing technique 

International Institute of Biological Control (see also Commonwealth Institute of 
Biological Control, CIBC) 

Insect Identification and Beneficial Insect Introduction Institute (ARS) 

Insect Identification and Parasite Introduction Research Section/Laboratory/Branch 
(ARS) 

International Mineral and Chemical Corporation, Libertyville, IL 

Indianmeal moth 

Institut Nationale de Recherche Agronomique, France 

Intermountain Forest Research Experiment Station (INT) 

International Programs Division (ARS) 

Insect Pathology Laboratory (ARS) 

Integrated Pest Management 

Insect Pathology Pioneering Research Laboratory, Beltsville, MD (ARS) 

Insect Pathology Research Unit (ARS) 

interregional cooperative research project 4 (USDA) 

international unit(s) 


. International Union of Forestry Research Organizations 
. Lymantria dispar (gypsy moth) multiply-occluded nuclear polyhedrosis virus 


Methods Development (APHIS) 
milligram 
milliliter 


. mycoplasma-like organisms 
.. multiply-occluded nuclear polyhedrosis virus 


mountain pine beetle 
macromolecular protein synthesis inhibition factor 
millimicrons (wavelength unit) 


. North American Immigrant Arthropod Database 


INA ets. National Agricultural Library (USDA) 
NAPPO ... North American Plant Protection Organization 
NANIAD .. North American Nonindigenous Arthropod Database 


NASA .... National Aeronautics and Space Administration 

NASDA ... National Association of State Departments of Agriculture 
NBCLY: National Biological Control Institute (APHIS) 

NBCP .... National Biological Control Program (ARS) 

NBCSI .... National Biological Control Service Institute, proposed (APHIS) 
NBRF .... National Biomedical Research Foundation 

IN GRE: North Central Forest Experiment Station (FS) 


NCFES ... North Central Forest Experiment Station, St. Paul, MN (FS) 

NCAUR ... National Center for Agricultural Utilization Research, Peoria, IL (ARS) 

IN aati sa Northeastern Forest Experiment Station (FS) 

NEFES ... Northeastern Forest Experiment Station (FS) 

NFAAT ... Northeast Forest Aerial Application Technology Group (FS, APHIS, ARS, PA State 
Univ., Univ. of CT) 

NGIRL ... Northern Grain Insects Research Laboratory, Brookings, SD (ARS) 


INTE 2. National Institutes of Health 

NIST. non-indigenous species 

INOYV cea. non-occluded virus 

i ae National Program Leader (ARS) 

‘st A eee National Program Staff (ARS) 

NU ee nuclear polyhedrosis virus 

NRRL .... Northern Regional Research Laboratory, Peoria, IL (ARS) 

OB ee ets... occlusion body 

ORO ge. hi. Office of Environmental Quality Activities (USDA) 

Ua Oia aes Office of General Counsel (USDA) 

OICD..... Office of International Cooperation and Development (USDA) 

OIRP’......: Office of International Research Programs (ARS) 

OpMNPV . Douglas-fir Tussock Moth (Orgyia pseudotsugata) multicapsid nuclear polyhedrosis 
virus 

Pier, os open reading frame 

OVA. te Office of Technology Assessment, U.S. Congress 

BU Vase to: polyhedra derived virions 

P.L. 480 ... Public Law 480; Agricultural Trade, Development, and Assistance Act of 1954 

(i Pacific Northwest Forest and Range Experiment Station (FS) 

BPPDS...... Program Planning and Development Staff (APHIS PPQ) 

PROD, 3.035% Plant Protection and Quarantine Programs (APHIS) 

PPRU .... Plant Protection Research Unit, Ithaca NY (ARS) 

PRG. People's Republic of China 

"Ny [eee Plant Sciences Institute (ARS) 

tA ee ae Pacific Southwest Forest and Range Experiment Station (PSW) (FS) 

eRe ss ass Pisolithus tinctorius (a myccorhizal fungus) 

MAC... 4. Recombinant Advisory Committee 

1 aes ia Rocky Mountain Forest and Range Experiment Station (FS) 

RMIS..... Research Management Information System (ARS) 

RNA ..... ribonucleic acid 

ROBO .... "Releases of Beneficial Organisms in the United States and Territories" database 

RWA ..... Russian wheat aphid 

RWUeh. «.: Research Work Unit (FS) 

BAAD i. spotted alfalfa aphid 


543 


SFCIML .. 
Sf{MNPV 
SIBCA .... 


SWsl 


. South American Biological Control Laboratory (ARS) 


State Agricultural Experiment Stations 
Soilborne Diseases Laboratory (ARS) 


. Systematic Botany, Mycology, and Nematology Laboratory (ARS) 


spruce budworm 


.. sugarbeet wireworm 


Southeastern Forest Experiment Station (FS) 


. Systematic Entomology and Beneficial Insect Introduction Laboratory (ARS) 
. smaller European elm bark beetle 


Systematic Entomology Laboratory (ARS) 

scanning electron microscopy 

Simulation Environment for Research Biologists 

Special Foreign Currency program (Foreign Agricultural Research Grant Program, 
Public Law 480) 

Southern Field Crop Insects Management Laboratory (ARS) 


.. Spodoptera frugiperda (fall armyworm) multiply-occluded nuclear polyhedrosis virus 


Subgroup on Introduction of Biological Control Agents (USDA, Office of 
Environmental Quality Acitivities, WGBCA) 

Southern Insect Management Laboratory (ARS) 

singly-embedded nuclear polyhedrosis virus 

Southern Forest Experiment Station (FS) 

southern pine beetle (Dendroctonus frontalis) 


. sweetpotato whitefly 
.. scanning transmission electron microscopy 


State University of New York 

Scientific Working Group on Biological Control of Vectors (United Nations, WHO) 
Southern Weed Science Laboratory (ARS) 

Scientist Year 

Technical Advisory Group (USDA) 


. Texas A & M University 


Terramycin, oxytetracycline hydrochloride 


. Trichoplusia ni (cabbage looper) multiply-occluded nuclear polyhedrosis virus 


Trichoplusia ni RNA Virus 
University of California, Berkeley 
uridine diphosphate 
ultra-low-volume 

University of Missouri at Columbia 


. United Nations Development Program 


United States Department of Agriculture 
United States Department of the Interior 


. U.S. Grain Marketing Research Laboratory, Manhattan, KS (ARS) 


Union of Soviet Socialist Republics 

ultraviolet 

viral occlusions 

Virginia Polytechnic Institute and State University 


. Work Group on Biological Pest Control Agents (USDA Office of Environmental 


Quality Activities) 


. Working Group on Natural Enemies (ARS) 


World Health Organization (United Nations) 
Washington Office (FS) 


. western spruce budworm 


INDEX OF ORGANIZATIONS AND AGENCIES 
Compiled by S. M. Braxton 


Units of U.S. government agencies are indexed under their respective agencies; e.g. U.S. Department of 
Agriculture (USDA), U.S. Department of the Interior, etc. Many reorganizations within the various USDA 
agencies have altered the names of many of the locations mentioned in this history. Names listed in the index for 
ARS laboratories are given as in the text at the time of their existence; the names of Forest Service Research 
Stations varied over time, and the most current names are given in this index, which may differ from those given 
in the text. 


A 
POOLE A DOLALOLICS cee tte te a tte ert ee ea ade kOe ates MMR SS AS baa ews 281,3107320 
Agriculture Canada (see also Canadian Department of Agriculture) ............... 0.0000 e eee, 152) 162 
Eve Pe UL ieE) VESTN aa rss oe nem) eee et Lede ee I Rees SoS oe cd pw pnw nts edu i OO 152 
All-Union Institute for Biological Methods of Plant Protection (USSR) ........... 0.0.0.0 cece eee eee 56 
RIC Ae VAN A eee ede OE eh eee ena cece fe ese ees Salk d cub Lech b ne wee 302, 304, 307 
PEE tieate Vi Osc OUTEORASSOC LaLIOM ae sine on 2am oot od, 2 ni ce eRe np AN ioe ISLA Gie 4 296 
Emerica’ DytOpAnOlOSiCcal SOCICLY, 4... eater ey. Miiaer + bee ale Ol, SS LIN. S Seis UE Sas 97 
PMINeLICam SOCIeCyVLIO HOMICUUral SCIENCE LASELS). Gia oui tere oes ORNs MOR ie SAB 40 
mmerican 1ype. « uire Collection (A Le O)sRockyillesMDiyweae. ©, . haw Lite Aba ao bet seb os 437, 464 
eOtCauuoe ALC ioe APrICUNUTe mara ei ote ciara ae oniaegase nehake sun SECA Me Gare Lee AONB ols De ot 331 
B 
Binational Agricultural Research and Development Program (BARD) ................ 00.00.0000. 98, 99 
RDaOV AOU. AE COLNAD +) pnctare es aes Cea caess SEN yA SP mae rr ctl ata by lie sh anteenah@ bn he 464 
ac COL DO st Olt eewe Pea, Lhe Pee eee he pid nis Gace ne CL eyes le Heam. 0 Wmnreied 319 
POLO ICAI OMIFOL DIVISION (DTOPOSEG)| gimp mune bsere cin oar MERE at OO I Mil todos ld aan ahs 154 
Biological Control of Weeds Subcommittee/Working Group (joint, USDA and USDI]) ................. a7 
ers RING Wee eee en nc ce a nt ea Aarne Coals plwatee = SESS HOW As: iinet. 68, 287, 308 
erdeallx WVivCop lasing COUCTESS. ety bu abe chau tiois tae asta x Re tae sroeitlh, wetlarw es wage 305 
C 
MlOriia Aor ictal EXDCHIMENE SLAOUSt sg «geben aie se, catgsts nies « rss ease ls v=. Wy Sakeck | eel 18259267 
(SUSETINY? Ls amet len came hia Phe Gee ol RES i re cca ka 2 
Ce Sle mem) er rer ts eee RNR chs ela shy Cena th = dclofac bel wis bie lesa. ile ahh le ons. Beare DS 
Poltormia Deparment Olt SIC UULG yay ta adam tenia te sees eels vs lat Ie ete de PREG 7 
California state Deparunent of Food and Agriculture. )00 eee. 2 nee sees tee ew gens 80, 266, 268, 269 
ee aitorniia staemoeparunent of PUDIC HedM er tsa ed cate eee nae ae ns seo ne Rake ad dle nid ess 276 
ined. OReCEOE LC OMIT Ol, PLeSIOs) ute cies etree ele shetty aian ec erie Sila. DME NR HUES fda 276 
Canada/United States Spruce Budworms Program (CANUSA) ..........---00-+05- 103, 105, 115, 445-451 
man aiiat Denarsenoat Pisheries and FOrOsiy : 0). \cclatetelesnedi- cogent aepohen e ac ad wen T a UMRN) -Ealelitznec eins 0 ee 440 
Canadian Department of Agriculture (see also Agriculture Canada) ..................---. 16, 20, 34, 453 
Bee OVI LIN VELSIEY rapes ts Miver dari. mo eret)ad ieiedin Spec nendy, ait a viils i Walinaalletaarg SEM OMMS SIEGE «bivlels 133 
Centre International de Recherche Appliqué et de Développement (CIRAD), France .................. 331 
Mmenese Academy Of APTicultutal SCIENCES, ns sect reese shee glna Sate eR ae Ohne spans Meee es 56 
“spy Tecretora ey Tfaree Tecate Peete Gly Ia ieee Gree ace oe et Meee Ak crac eo ane ee 304 
pa (relay COMpOrallON ce a ho atn. , OT Tea Se IEW ev Eas Pen wen MN e PHU NS Pd ew ee 96 
Colorado Agricultural and Mechanical College ..........- eee e eee e eee eee eee eee 396 
Colorado Department of Agricultre .. 5... snes ee ee eee tea ee eect eee ete eee ees 84 


Colorado State, University ce cihstskias j, ony aetna Alec syetete alte veuman meade arias satel cane ane nin emo onahen teen eet aes 396 
Commonwealth Institute of Biological Control (CIBC), see also International Institute of 


Biologi¢al’Control (IBC) 4 3 segme saat eta mueen nels eet a bee ak rte aerate 60, 84, 85, 261, 417 

Indian Station. 20. 2s cies cea we och tee lat py omtaheiin niles ey eycpet anal e anealtoh ice Reite co 2 tel eons ets Cnt ee 417 
Commonwealth Scientific and Industrial Research Organization (CSIRO), 

Australia : eee Ree eseshes da tue a tee olzee be usin ta ae ete estane ace tahin ee oker eee fs eee nena 70, 86, 88, 314 
Connecticut Agricultural Experiment STation, New Haven, CT .... 0.00. 00. ey gee eee 420 
Consortium for Integrated Pest Management 

Soybean, Subproject 4 sacwy areryaan AAS Gee Ue EAN ee ie tie a eget en 57 
Cooperative Extension Service, general (see also under state of interest) .............-5.0ss0 esse eee 68 
Cooperative Forestry Assistamce Actiofl978 ie <i cra aia cue tere © eish ore Rlate tele eee Noles Pan onc ean 107 
Cornell University. Joc os tie eden oh etna eetels, OMMN i CaRat a we neater Cet ee eae Mey et eee 99, 312, 314, 426 

Boyce Thompson Institute for Plant Research, Ithaca; NY... 22.0... 50h. cee eee oe 312, 314, 330, 426 
Crop Getietics International: 22.207 Reis owas obese ciel eon ial spot e igi ote tatters) ode) Slay a) aa ene cetera 92, 437 
D 
Direccion General de Sanidad y Proteccién Agropecuaria y Forestal (Mexico) .............0.0 eee eeee 153 
"Division for Biological Control", proposed establishment within USDA or EPA ................. 152, 154 
DuPont — <2 Pe duisiers ee hug Steals Rete whe Paar ah Sem dain 2-48 ccna fa ec acre ae ee ee 437 
E 
EBCORED) sii die 54 biel ge tw get oy eg a emp Wo wk RD & Cad 6) oa er 1s SERRE REA ee oh 
Ecole Nationale Supérieure Agronomique'de MontpelliersFrance 2. ..97.//iy ane e ol ee eee 331 
ECOSCIONCE 4s. 505 Gia le etal Siictals CRAs ge Gael Balls Wee Ro MMS IRIS even seRlae oprete be Senn SUPE A Eee fe es ch err 98 
Entomological Society‘of America; 20 0e cei ete hale ee ye 5 ww oo tee I se ge eae ee 53 
Experiment Station Committee on Organization and Policy (ESCOP) ...............0...0. 000+. neue 152 

Working Group on Biological Controlws..c% os... seh ciertie oe ene cle ee Re 152 


Environmental Protection Agency, see U.S. Environmental Protection Agency 


EsprowInc,-Columbias MD tp... stccs dire aie oevs oo. Sitcvood toae Eiepete ie Meanie ua Je ctisatt chai nee ae at le nn 437 
F 
Florida, Biological Control Laboratory (FBCI)ii5 = Wes Seer ote ne er eo 57, 58 
Florida Department of Agriculture and Consumer Services «22. .55- ass «+. sh Jeon ep eiety ennne Be 
Division of Plant Industry S214 SURI e «x ternens boca ctsdeloqseiacsccscsanealraake cane Gas eaee 7 eae 127, 144 
Florida Department of Environmental:Regulation Ge a. c-cd eee cio) ae 79 
Florida Department of Environmental Protection @saris) cy oe one eet ee ee 79, 80, 87 
Florida Departmentiof. Natural, Resources iapnn ie irre vt ee eee etalon ratep dens Geta sea ene 79, 87 
Foreign Agricultural Research Grant Programs: 320562). cece «ose sien oc oe aR 2 ne 25 
Forest Health Monitoring Program (EPA ‘and USDAIFS))2,. Gass 0 eee cee ee 105 
Forestry Canadas ji). og ts wiser sly ab boarsuni Sahl <cagrebr ag aleeerccs Min aatie oe Una lara ease give eine a 127 
Forestry: Department (KRemya) 372.51). tier. ee viene ilet uc oavs fells cis lage, Beets coil eee Ue 108 
G 
Grasshopper Integrated Pest Management (GHIPM) Project (USDA, USDI, EPA, and others) .......... 313 
H 
Hawaii Department of Agriculture 0): dcc./saa pis acieccicicen ciel) ois Ue. ent 4, 466 
Hawaii Department of Land and Natural Resources :2/2%) 20s sililsies o yelocirinie) Svcs ene eee 466 
Hawaii Volcanoes. National Park jh... 2.cctosinw abuse cutis es ple Moet «On eee 1 eee 466 
Hawatian Agricultural Experiment Station’: 3) iciee cts sie faite Sey se iil eta elke Oke ee 17 
Hawatian Sugar. Planter's Association. 1.00 2 orcs cre cicte snes oistc! ie svoeasafesaielat lanes eucetes sane ne ne 4 
Hawatian Sugar Planter's Experitnent’Station Waa mae esa Weeds) cui cece au tan een te ae ig 
I 
Insect Pathology Research Institute (Sault Ste. Marie, Ontario, Canada) ............. 0c cece cece eeeee 299 
Institut flr Spezielle Botanik (Switzerland) © 7.4.44: 5 «ace a een te rte 89 


546 


Institut Nationale de Rechereche Agronomique (INRA), France .................005. SA 2 a0 2329-35) 
PSICR IG AU SOTTO CS@ALCHTCADOL LOLLY eaek an Siam Bie Ahad cic a 4p Sorpedilsy ivi cary a bub 8 dutivvg, Wiad’ s, whe oe an 329 
Institute of Forestry and Wood Industry of Serbia, Belgrade, Yugoslavia ............... 00.000 ee cues 417 
Interagency Biological Control Coordinating Committee (IBC*), see under U.S. Department of Agriculture 
PprermatiOnaleA toric Eherey Agence W UV IGNOA A USITIA) i cic svc + cc 5yo5 Siac ea wieivate ob ie weed oe eas we 271 
International Cooperative Program on the Spectrum of Activity of Bt(BtICP) ................... 320/321 


International Institute of Biological Control (IIBC), see also Commonwealth Institute of Biological 


CEONITON CLE ee ent tn emt PRE toe aS ss kaw es 83-85, 106, 123, 125, 152, 153, 454, 455 
international Minerals (and Chemical) Corporation (IMC) ........6. 066.60. c bee ec eww ae 309, 319 
international Union of Forestry Research: Organizations (IUFRO) «........5.6:66 6 acen eens ane mnavmans 459 
Ht een COL ETYEO VC Sees mre ean ney pee IE EMCEE nc 5 wi ul se! Slangin inte Go Spa nied > sahigidle Ablae Ceduna y 98 
FETE SUDETIOLS Cl DanliCatiny Cxelalemltaly sete nneiers Ghee soy Sica Shs pews Wa Sind a edule tbe w lew oaeEO es 87 
K 
ROTEL ON ESI ULI PALtIe NIL Cmte reece opti tne Bin 3. 0s oo, Geom is) oh chro Gpamcl nga) oP awa Quod aap ea wre Gua avi eheee 455 
RCRA EOL OS LV a, COCALCILUTISL INIT Cami eened Wer teen alto sg Aa tae tes « 45 nigerian ees GE (swag absent wis ete aha? 455 
Rca SO) Cee Men eT, RECIPE ET er tes es tee ss Wishes aca aigusee ‘Bigecel wie wyaiys, didi ac dlptie od Wee Db ed 293 
L 
ROHS Palen ys ILOON WO SA SSOCIAUOM ier sie tigi n giie 2 se Sox Hci IRE ove adda ahd © ajo lelw 2 oe age 293, 296 
PCH TISERIVATSYUALO TO TLV CLO (Vereen RN NPE Pal ee es ingen pnarguanien sS/aiteand Pg bc mae ie oe sone 295, 406 
M 
RA SEMIRTCH IOC Dal INET Ole’ CTICUIICUT CEL, myst dietge aia as a hiss se atest 4.4 one So's mm Rane >, » 60, 76, 83, 121, 423 
aay AARON Se OArLneNs OL eULAtiSpOltaOMmy eta hh nee pia. s Sots eg auMMN te 2 ci gael se 4 9 4 Ge ks ececom wiiieton 83 
Maryland Gypsy Moth Integrated Pest Management Pilot Project ......... 2.0.0... cece cee eee 423 
Ministry of Forestry, Beijing, China 

Pe TIE Se PA CACTI ZO HOT CSL Van ye arn iCute ayetitab w eist tre ace eer sl labinsn? daa)eaacap Uo Yeap tan'e Wavy vpn acts 420 
le oe sea i ALemeO ere NIV GESICY Ueies nate taye i hela Gi Sig Prt mw udsorsie) wars Au eiwis en Slale pada Wek) Pb 
Rear m Oe pat cmneny Ole. STICU LEC acta eset re obs hin ec ioke aga eteyWatangs «VME a ied Coa ss ws oe aaly iter sive dod De 17 
REC PRE OCR S EVO UNIT VETS IC VOR Omar, eRe atm Mant oy iat liy ae: sn. et -iefeevng bn arlsIAVAOM wera. bw Spmaghiss® Sodio Rois 122 

fre ite Te He Se Are th CCTICOs Bree Pieri tke art Sendo Shs Nseries ade us ehah rach ier tye RD Se ao yar ee 415 
Pere sts SIOL CALE Ms TIRW CLS ICY mre M Tet ey eer isi oak cele Aiptciaiial hy Grapmanre 6 Sou! b 6 HA Ge pulled ewig Nal Lae daisies 408 
aeeatorsaT CCE COLIN AYLV a MORN ree EI cece PUN hays he once ity) sete ar Sle wre idl atc he] Site Suns ad ty 6) agne'e Waa sae) Seago al ee 95 
area HAE INARSUALORUUIVIVEUSECY moe ctr reus he yet amen he) tA csc rc csk wh aitdy ® Oar that 0 AMY Degsieliacds wnt fe 53, 76, 78, 79, 85, 89, 148 
Bear re TiO COL AL ON Mmrees 2he fe IN AES hd sacl eae ahi soe te "ems doe ghahajsi gM aNeiame Gita a wee eae 32) 
N 
Rin eniawe CANE IOT SCIENCES er tent sem Cae: str me RIE ah So wines teal e + «Sieben RAM Be «wi 2, 48, 98 

Committee on science, Engineering, and Public: Policy (COSEPUP) .......0. 0 eu daemene vee cane 48 

Research Briefing Panel on Biological Control in Managed Ecosystems ...................04. 48 
Nanonal Aeronautics and Space;Administration (NASA) 2... os ci eee vows ye meee vem eta 299 
National Association of State Departments of Agriculture(NASDA) ...................000005. 124, 151 
matnnaloasiminesister company, Davion, Ol wat an nega cays § co oceans hese aries ye dotnet abe vin panels 319 
National Institute of Biological Control and Beneficial Insect Research (proposed) .................... 49 
Pere OU aWmTiee enter O ts btea th) (NILES henemente Sve oun Ramat wee, oats oyu a eacuaun, sha e suen Pek meee eawia oan wa 2997305 

maimoenes tomuse of recombinant DNA products) 0.5 cisceia toe ine doles acne a ye ae eaes olan we 322 
Siatiatal Parimersiit ton B10 lO fiCalOUrVveYy | PIOPOSEO is a cies Slee sae ees Oates adie disle ne ee vis 155 
Co eeeiyeth PBS SYe Re yg oo ks pee Sie PN na Me aM eae A 134, 144 
eae oC ATC IN Olive Ime Me Maa aed cy, hie Sn ballep otros GW Otay doy talents <olety aga Ota ad a aloes 40 

MEI ASLOVITO PLES Int) ANG A OTICTINVIEG eka tia iol sina 5 6, dls. 11% 5 sia = aha tegnnesk Mien tl dias ones joe obs Sia. Sa 40 

Committee on Biological Control of Soil-Borne Plant Pathogens .............. 0... eee eaee 40 
New Jersey Department of Agriculture ................... LO 228 sre Ole Or S42 eS], 144 
meen and institlicu Ori TOP) anid: HOOGIRESEATCH wi nac Sa ses ele cle va vn a a 6 oo arg be eae 99 
North American Plant Protection Organization (NAPPO) ...-.. cece cee cn ee te tee eee 1525153 

Brmlosies ee OnuOuranelmeny = aren ten, (ae ORs. Che eine Hes Be esa G ea wa litedie a8 din ache 13 
REE OH Va MCHA mMentOmA CriCUILTe ey ca ciotstayin accion fe oe > 2 Walelé we ceed Fae ne vale ee oes 53 


North-Carolina State University ifs, <1.) cone teste weeds ose gee vies ls ee eae oe ce ee 62, 423 
Northeast Forest Aérial Application Technology Group (NFAAT)=< 2020. esse oy et ee 430 
Bt technical committee 5 cia 5 when entree tinct gs ue. ya ok meh cherie eee Gr och: Oe eerie ke een 430 
Northwest'Seed Growers ASSOCIatION J. crac conn fs 6 gen cs cerns alter ot nese vind Chere ate ae any 324 
Nortliwestern State College; Natchitoches; AS. 9 20.8 cee ter ate es ee ain ee ee 406 
Nutrilite Products;-Ines. Buena Vista, CA rere ccterrcns «carer ter act hawt) een Rte oct ae e Ree 319 
O 
Ohio ‘State! University 22 5...cis 5) 5% Beck Bid Gudea teen dyelc crane sfc ciel Oke enenen Catecee te eney ae eae 303 
Oregon Department of Agriculture 2. W2 cay Wa taie se pies ws Utesiete gn sce vist ee ee ensuite enter een eee 38, 84 
Orevoti State. University is Waris ni oiecs opt crcia dene ste oe crcont aren hr arcaces caer att Cun ke ee 38, 324, 396 
P 
Passamaquoddy Indian Tribe: osic snc ogaued asta Ace ate tars mal Moura sos eleven geke eee eet 450 
Paster‘ Institute; France 6.0 ss Sakae canna cee Sneed Geog ells cade aie oho en eae 314 
Pennsylvania Bureau of Forestry®.35: chen os taes eons eee oe es unite cette en) een 67 
Pennsylvania Department of Environmental Conservation, Middletown, PA ...............0.0 eee euee 420 
Biological ControliLaboratory eens re cet: eee ee eee 420 
Pennsylvania State University ark. . teat cen een cee soa aie kis eee ee 98, 426, 429-431 
Pesticide’Research Laboratory: ~s.0%, see ee. oe eh eevee ea eee eee” Cea ee 426, 431 


Pesticide Research Center, see under Michigan State University 
Pineapple Experiment Station, see under University of Hawaii 


Pineapple Research ‘Instttiite 45 Grates Sic cara i elaemad, Cee, o hceukl oe eres y rum a a ee i 
Polish Academy of Agriculture 

Deparimeéent-of Entomology 2 ix acacia ne coe eeu eed, clic re pee ony en eee 330 
Purdue University’: 5 .ahc wa vie dices ae oe MER ne Mee Cae Gee aes, weyee aeeylorlne tena ake eae ee ee 122 
R 
Rio Grande Valley Sugar Growers Associations 234.72) os ae «et © ue eee ee ee 128 
Rockefeller Institute for Medical Researchat Princeton’... sen. ne ee 19 
Rothamsted Experiment Station, England? 32,4.) nse tae rs ee 92,314 
S 
Sandoz; Trice! San Diegpo PCA ca sen anes ayer ites ce ees ce Snes e 304, 308, 319, 327 
Servicio de-Plagas fF orestales! Madrid" Spainte. ce. k ccs eos ces ove ee ee 417 
SFC, see Special Foreign Currency 
Sino-American Collaborative Biological Control Laboratory ......................05. 56, 82, 89, 92, 149 
Smtisonian Institution Washington, mG yee. hyo. ate cc toate ose tle 299 
society of Invertebrate Pathology ick eS aude et eos Sela ac encase eters sete ee 299 
pociety-ol Nematologistsm:, ava tgst Stee to ake wat camel ee ee tire oe et ne 40 
Southwest’ Florida’ Water Management Disthitt ... a2)... 5.0 o-oo can ee ate ee eee 80 
Special Foreign Currency (SFC) program (see also Foreign Agricultural Research Grant Program, 

and see Public: Law 480 m'subject index) ee ee 25, 37, 39, 46, 56, 80, 82, 151 
State Agricultural) Experiment Stations (SAES)= 9) eyes as Lec eee, Fe ee 4, 151, 152, 260 
State Departmemtsiof Agriculture mn, crac arn. | ar eure eae ee eee 151, 260 
State forest services (general, see also specific state agencies) |. se 403 
State University of New-York (SUNY), Stony Brookis. a. set tt ee ee 305 
T 
Tennessée Valley Authoritya eee teae ttn crc as hae ee ea ek ere ee ee 260 
Texas Agricultural Experiment’ Station. (3 nc Sn see ee ee, ee 27 
Teéxas A°&.M University (TAMU)2= sree oe ae oe ae eee 52,05, 03, 124, 128. 2808320 
Texas Forest Pest Action Committee 075 a. es ec ee ee ee 406 
Texas Forest Service 72 0 linc aste ts og tes trae tae nates ep ie oe ete Cee ee 407 
“Thomas Committee" (see also "Thomas Report” in subject index) ............................--.. 142 


548 


U 


United Nations 
Deve ODmCHOLLORrAlll, 4, eas peice hoe Ne tein ee See ty we tose 106, 107, 454, 455 
Pood andevcncutureOrcanization( PAO) iin... 44.5 is tiahee Wes OMI G a. Ae ke 107, 455 
ODIs eat realisation ( WEtC)) mre Wa hc ae. as «da vi Rees Cas oem biota 294-296 
Collaborating Laboratories for Pathogens and Parasites of Mosquitoes ................0 0008 295 
Scientific Working Group on Biological Control of Vectors (SWG/BCV) ............... 295, 296 
PeVeTSidane | euerale;de MiatOMFOSSOMGUIADANNNIE ET, Gs oll cwalec os c5c oe nase vole vane vadmlea eels s 286 
aimiversitiast CCheralsseeralso specitic UNI VErsIties imam oh sci ekie Oath tyts ia. see lem. 403, 462 
Per versitvcGt ati ZONd mee eeeeen tee ere Pn WS gle cates « «as SORTS ass WM aa st 293 
Sei Versity i AT KANSAS bye sneere eee eu Arn Cree clo. His Fed! 28 a RR eh a rt 62, 88, 144 
Rivesnescarc inane ntensiom G Chtonmen parative i 2% au biol. &. saree SAWS. Gate cies 2 88 
Serer ta] hy om ei COTES memrmt eni ee ret yet Wom Mem onde oS. doe of sh a Wein. sax sgh va EE RE Ass 2 dow lca oe 331 
Liniversity of California yin aas sou estar al OFA 2055 17-2.1825528, 2933-35) 40N50952553) 58, OF, 
68, 70, 76, 84, 91, 94, 266-269 
BCrKc lO pee wre ern ei rs Pale ed AL We Ee. De ee wh. UI RESCN AG 29, 34, 70, 276, 433 
DepartmentrofeelantRathoocvare mat. eee sake kL ol se, Ame Ye RRR es 280 
PE OONELAIV CH KICISIONISCEVICC MMM mnt wien, Suet aon a's eter aNe aus nt ea MR NIN 6a gale wee 68, 278 
DAV iSareeyae ee rates ev ec eed tae Rhee i ced GYRO Wo ena OELERRG SB 91, 287, 452 
Pencrimenvoubiclocical Controlmemr 0: yma ou ois 2 sae sacs pps 8 4 be RRM bod ng ee Ss 15 
Mosuiiea Kecearen-aporatory, | rosuOn@ Ane araretninigita oor tock hi ae dee es ee Mae. 294 
RG Crist) arene eee ee Tee RM Py eNe Lachele eekT Et: S2yiir ENERO Sala Hae eid cs Ge AR RS 266-269 
Riverside pee oy eer a eee Soa tek Modul Cee VW AO 40, 144, 279, 281, 285 
MIMeroity Ce Onne CHCl LE tim wrens, ae meee. hy iia. Lieu. farce eel ae 430, 431 
Perestmyicrcormocysicescarem PlOveClare ©. sete twee as deta thee co WAP mn SAAN e led Oem @ 68 431 
Piiversity,on Florida, ayaa sk ade sok ee 40, 50, 53, 77, 79, 80, 86, 135, 144, 285, 286, 295, 408, 433 
BeICeraif On GeOlgia AcUStmre amen nee Moran ha M ened Suton ced nae TNA Te, ae ee Ae 455 
SEE e TOL ACCEL AVAL WRN eR fete tl aie Sea lela 2 te Sst ood cw el Se SEEM So Mere i See kp Be 22, 466 
EC oN Oled RDGIUNCL a tAULOM MNP net GIA Bird ale b teas. F gees Me MEA cde eS ae oe ey Pate oe 22 
BETES Va ECAC eee ee ort omar etna «ois cls Cs SI Sb Ray Be, 83, 324 
PTV eesity 70 1st de mene perenne we Nee ap tee he al Peles § SORES APU Pas 6 RA REGS B os 133 
SCOPE Mey ame ted Seema re, Prete nH One We ne cals Cae oe ag 5 vie SRM hate ee UG, Ye deacon 12 
Peer et Sit GIO eINUCKY Ce RIN At OM Ms Laer ier cia a us «i Sh uant B1. SIRENS ee Mulew NS CER Eee il, 452 
Bir eoesicyT OF Viale ONONU ME nev he, Aronia ak 2... hdkia ait dete Sein te Wang Vote eels 445, 448, 450 
Sern T St Ot VIAN VERGE aint Sap ereion eae ee inal aero hy ale Neteh  CR LE es SE 60, 121, 302, 422 
Ser eESity a) MASSACHUSCUS Mere n mine eta me As nee. cttie Mee ct unene at Rael e das oo ewe fateh 130, 421, 422 
OS OVGISSILOAIY CG MLSS 2 gr Re ie ee a ee ce 439 
Pmmrersity OL WitseOuria. ColUmoidt UMC jit 2 eventianemoe sal oeul ys Oe. a aea tl ones Helge ire ae 307 
MCUs it OL NC DEAS RAMEY eR Tit uh HAIN he cidiy ost AL ee ct Me A AN eae DE eM SBM dae A 412 
BE DERSILY Ol NOWEIIOKICO Rey te) Senet nen iia aaininain met unl a aay BM ed Deets AMER RS Be, 4s 404 
Seat Te ICS EPI CVEL TAK Ae Wrenn BAe) rvtod dade ali. vata dice ica RB nd natn Maho s SUE ose aod 427 
ts Ore TON eee Met aie Tes oa eine aes MERI IT OIE Aa Lk Be MO bes ee ems s2 
velo FRENTE AUS Pera PCT EY TaD 20 Ace 2 anit doy rc a Oe ec Ra ee ee 330 
“SEIWSETY GN PIUTET Ts 3 oe Se ne, Fn nt Ft rene ea ee ea ar a 294 
eee ORY CLITON Hemsted IRIN NE. Gels clvie wisi. odes ire open nisin ween Tei eR ee ee TAC UN Gea aga 422 
Beets ey SCOUSINM tM a ci bear one aves oun homie See mnaauhe yore daar ome A UM En ee oes 144 
ee siry Oey ONIN Oe tits oe ys een POR hte LETS oie Nie Shee ne Das PPM m se ele 328, 329 
mee ccne, aor Intermational Development (AID) \c2vtiwe Moti ie oP es Ue la a Oe oe we 285 

U.S. Air Force 
CCITT, TANNA) Ot SPS nl Ot) ae a a OE a See ne), 293 
ace ieNalional<uard based ANGB), MA Sic... 8 aa awed Sy ORL ee eee 121, 126 
US UNSER Roo ase) lt olst: Raat gh) SPR Ge aR A Cece 302 
Beemer corns of Engineets, (ACE) Gino tis oda visi vss ve tlows aeeuelaiene st 38, 39, 79, 80, 86, 87, 149 
ouaeelant onto Research erOgram es vas. jn cee ito. wees oe mee enon Meee es 80 
Saree AUIy GM EELUIMCN (IS aOM mre Mere Merger. toate a <r pct dln, 6 anov ab dlls ofcbals\ = MUD Win afin siedal gale oa ole a 80 
HES aC ONOTESS Neds teste cisiris RNS 40, 44, 48, 53, 102, 105, 106, 109, 111, 113, 115, 124, 268, 402, 418, 433 
mrieccromlechnology Assessment (OLA). 06s. tei nu ve tenia haale de tie aie y we dlewlaine « Son oe nL Sa 


549 


US. 


550 


Department of Agriculture (USDA) 

Agricultural Marketing Service... 25. 265263 fs neues sts deen eed tok ee tel ne ng ere eer 25 
Agricultural Research, see also Agricultural Research Service ........... 2. eee eee cece eee ees 46 
Agricultural Research and Education Service (ARES) .. . . 00.05 5.) ieee te es tance 48 
Agricultural Research Administration. : | i.c).ae cc 2 on eo ale mre ee neta 1832052125 
Agricultural Research Service (ARS) ........ 2, 23, 33-43, 44-99, 101-103, 120-127, 129-131, 135, 142, 


144, 145, 157, 164, 165, 260-262, 264, 266, 267, 269-331, 
415, 418, 420, 421, 424-426, 429, 430, 442, 453, 466 


Agricultural Research Center, Athens,GA 7. ...\~ < . 2.0507 witeters vrata to erate ie <i heten ee ene ee 99 
Apiculture Research. Branch aoe $22. cj ct cce 7's 680 5,4 Win on win ee Mew ge deat fee 34, 297 
Appalachian Fruit Research Station (AFRS)o2. 3 5.45. ams es oe fees «2 sore eer 98, 99 
Aquatic Plant Management Laboratory, Ft. Lauderdale, FL (see also Aquatic Weeds Research 

Labotatory) Sos ¢ 24a nase ghee alo dhe cote © etd ei ie eee a eee 57.7 FAD 80 
Aquatic Weed Control Laboratory, Ft. Lauderdale, FL (see also Aquatic Plant 

Management Laboratory, =Aquatic Weeds Research Laboratory) ................... 263 
Aquatic Weed Control Research Laboratory, Davis, CA 2... 40 2ce S900 ss aie ee ees 79, 80, 86 
Aquatic Weeds Research Laboratory, Ft. Lauderdale, FL (AWRL) (see also Aquatic 

Plant Management Laboratory) <6..0 254.0 .20+% +> + =n ae anh ste ae Seance tne eee 39 
Asian Parasite Laboratory (APL) (see also under BEPQ, Division of Foreign Parasite 

Introduction) tec amet ain coe erence tie ce eee 50, 54-56, 59, 67, 77, 79, 82, 85, 149 
Assistant Administrator for Plant and Entomological Sciences ............ 0.0.00 eee eee eee 261 
Avementation Biological Control Facility 24... s gne n+. 6 dma ee es See ee ee 148 
Australian Biological Control Laboratory (ABCL) 20.0) em «scene eee ee ee 77, 149, 154 
Bee’ Biology and Systematics Laboratory, Logan, UT) 2s... sae - tn oe see eee ee 324-327 
Beée Culture Laboratory; Beltsville, MDs ic) Sven ese ee et ee 296-298 
Bee Culture Investigations Unit, Logan, UT (see’also under BEPQ) =25.. 5-2 eee eee 324 
Bee Disease Investigations Research Laboratory, Laramie, WY ............. 0.0. c eee ee eees 297 
Beéé Reséarch Laboratory, .Beltsyille, MDa 22 3 gene te > ree ee 296-298 
Bee Research Laboratory, Pucson, AZiew. <a.04. ac 2ous are > «0 -Seenetee Comer ne heen nn 273 
Beekeeping: and Insect Pathology Sectionie. o.-1. ans os ue srs ere at ce ce) eer 34 
Beltsville Agricultural Research Center (BARC) (see also U.S. Agricultural Research 

Center; under BEPQ) stem be srcte cients crete stove ee nee ae ac ah a 49, 66, 91, 92 
Beneficial Insect Introduction Laboratory (BIIL), 

Beltsville MD "art re ore omer ah opr eet cle Neseeea, Smee 50, 51, 62, 78, 79, 83, 149, 262 
Béneficial Insects Introduction Research (BUR). .n .2o.. ea es ee eee ele a ee ene 56, 60 
Beneficial Insects Laboratory (BIL), Beltsville, MD (see also Bee Research 

Laboratory). sc vive: gies oleae etter orn Be eee Te, us ge 8 Seah a ct en 51, 59, 83, 298 
Beneficial Insects Research Laboratory (BIRL), Newark, DE... 42, 43, 56, 58-61, 262, 401, 419, 423 
Biocontro!l of Plant Diseases Laboratory (BPDL) sn. oe eee ee ee ee ee 93-95 
Biocontrol Working Groups: 20. we aces ave sours w 4 os hela Gare emer ar ee ee nee ee 48, 150 

Microbial Biological: Control o7),t522 facies Ge wea altho ecie'sig mien aioe ee 48 

Augmentation and Conservation Biological Control ....4.....<.+..0.5-vuee use 48 

Classical Biological Control oa.c ews. Aare octet Ae eco s n c a ee 48, 52 

ECOIORY", fu. = 5, pate os ade o hmtevemedeaieel a itis a aurea exe te ar ae eat Lie ng 48 

Natural Products 3.00 ' psee atu aaah ais wie Dei duc ale ieee ie ae ok et. oe 48 
Bioenvironmental Bee Laboratory, Beltsville-MD 2. -....... 1) se 115. ene 51, 297-298 
Bioenvironmental Insect Control Laboratory, Stoneville, MS .....................00. 377815263 
Biological Control Documentation Center(BCDC) ............ 46, 51, 58, 135, 155, 156, 163, 329 
Biological Control of Insects Laboratory (BCIL) (see also Honey Bee Research Unit) .... 57, 63, 149 
Biological Control of Insects Research Laboratory (BCIRL), 

Columbia, MO i saan aw ee tee ee 25, 31, 56, 60, 63, 65, 69, 78, 263, 307-311 
Biological Control Laboratory,-Gainesvilles FLs..., 2444 to ote ee re ere 263 
Biological/Control of Pests Research Unit), 72... 424 524 ot ae Aen eee Oe ee 62, 65 
Biological Control of Weeds Investigations | 7.2.2 ou... -eeieane en anne Rtn 37 


U.S. Department of Agriculture (USDA) (cont.) 
Agricultural Research Service (ARS) (cont.) 
Biological Control of Weeds Laboratory, Albany, CA (see also Biological Control of 


iW Cede -Researciizaboratoryren Dali GA) fapeerenee mates GWE walks Vidi. aetna te. Gumedd =. « 262 
Biological Control of Weeds Laboratory, Argentina ...................000. 50, 54, 77, 262, 286 
BiolosicabContoliot Weedsaporatoryy Italy in ws « oh . MS ae le SY te 37450,-/6, 262 
Biological Control of Weeds Research Laboratory, Albany, CA (BCWRL) (see also 

Biological: Gono) omwieeds Laboratory, Albany;:CA)) skerct!, slimisad.. Wee ie bn bees Saas 
Biosystematics and Beneficial Insectsiinstitute (BBID ins sine laa is eo aed 51, 66 
Biveberryiand Cranbermy Research centers Chatsworth, NJ). 05 cn) Osh datas cleo cates ces 9 
Bow eevileeradicanomnesearcha nitakaleich, NC oon ein ase ceicinia See he eh wleieele ee es 62 
Boll Weevil Research Laboratory 

SLAVING RIV SMe eee EMRE T TER er oe AL Ov No ieee aC Weal so eM lana Mica Kum a SERRA 6 ds 295 

IMISSISSIPDi CAvC IVI Manne eee nale tery el ROR Whines ote As malts » oe 212 
Boyden ENmmolopicalileaDOracoryae myers rtttelees Sele eis ris Waheed achat Malian alee Cae 281-283 
Carl Haydem ice: esearci GC etitenmer semen mies ttt oy he hoe hes We Saale aa Wek Mids 210243 

AR opee HescarciADOTAlNry ia amet ts ee Nee 5 cao ess a ae hg a TR sia kw Die 
Collection of Entomopathogenic Fungal Cultures (ARSEF) ..........0... 0000000 seen 314, 331 
Coopertivers preetient Grantee ro grain wee anid eee A a ieteas dole St ee. Fase aba eleva a 236 
Cooperativers seatchin creementsmmn eee ier belt st diet ol nats CREM. Sa Rw 304, 324 
Grim Msectsmesearcn LINMMANKOMYCLA Gh Mi Sn ME niin Gna iccch ga. cients ie aot oiMW malate dis a's 291 
Cotton insects Biological Control. Vaboratory;TucsonvAZin: 308k ieee. Wiles eG tee es 262 
Cottom insects: Physiology Laboratory pape metre See Moras Sk ulate wa MR Sb ae 66 
Op onsnseécisdesearcn laboratory; Brownsville, TX so 24.5 ss4 due She alee ee 317-321 
Cottonansects. Research Laboratory; College Station, TX 2:4 vatiewh. POET) ae aa 62, 65, 263 
WotOneanolorVanesearenenieKCE RU) mi nate. ota | Ce ROE, sks etal. 93,96 
er OSEETOLeC MON CSCanCIM aig ae ig sisi. ole ahead Air Se one wi eete Os. MAGE eas 33, 39, 87 
ropa nccedtcih DEANCW IVISION Pei. t am: is 'o sae abe eterna Wkly Saha, Wik Sealey 39, 44 
EP rOpsesearcle ADOLAIOl Varin meres etna. hal gORMO el LOC Mninni ob Sacer Sheltie le 90597 
Current Research Information System: (CRIS) Work: Units, 22982 os te OS IS os 47, 67 
Poodraminta Protection ucescaren Lanoratory ffs. 0.7. on ee ne eect. RE Yada so 58 
Pasi Goast parasite Receiving station, Moorestown, NJ i.¢5. nese. ccesuSeNeee ee. oo 5d Dan2. 
Entomology Research Branch/Division ............. 23925,.33, 34, 36,.44,49,1219293, 297, 311 
Entomology Research Center, Brownsville, TX (see also Cotton Insects Research Laboratory) ... 263 
European Biological Control Laboratory (EBCL) ................ 8, 54, 55, 76, 149, 158, 329-331 
MiG pe AliCOrmsorei ADOLatOry, ANKENY, LA wane fie eaters io wins aie me he kaon aw ee 291 
European Parasite Laboratory (EPL) (see also under BEPQ, Division of Foreign Parasite 

Introduction areres 25: aa eke 2. 24, 26, 27, 36, 50, 52, 54, 56, 58, 59, 67, 72, 158, 262, 329, 330 

LNSECIRE AH OlOZYAL MiP ADOLALOK VM eee Mts sou ites! hace tangy renal ad acetone Naas as 5 330, 353% 
Exotic moun vasivesw.ecd Rescatci Unit erie tere as bce a das RENE ss. 545 4 149 
Pormentanemriology Research. LNitimnwumen qiceceas tr Senne: Se de a stems RNa so 90 
Poragelandiance, Research: Unita meee peter. (alt eey aia ee emt onellad TE IR RN Ns 6 oe 79 
ForcigmDisease-Weed.ocience Research Uniteniersaclsnmiceeetsnitin it ian ee eas lass soa sl 88 
Rr Cea OLALOV Va Re RL Ce ae an love NEN doe ale ete se aha abe hatte mlavegada s SB Ian eat 8 98 
rranmandioraceunsects DIanch yc. neers eee Peni atin. wattle. SURNAM le Weeds iw a 311 
GAs emO DSTA OLALGE Vie yh ny aise Seok (soe wh gh ND EEO Ret AO RE i AS a go yw os 262 
Grageid sol andi ater Research: LabOratOrysad ae Sides b tuc eehekate he MMB > alain a sees 81 
Gulf Coast Mosquito Research Laboratory (GCMRL), 

Pakev@arlesy Ae wets Meee cae cae oils what hv UE hie MAUR RE INICA. i 263, 285, 293-296 
Honey Bee and Insect Biological Control Research Unit/Laboratory...................... 63, 65 
Honey Bee Disease Investigations Laboratory, Laramie, WY ..................0005 324, 328-329 
Floncsapecemescarcn Umit sb ucsonn AZ, 5 deiiarac sm stan lets erin dns a deeoe mes eres Wige Nl 94S 57, 149 
Pome soce Meseatch Wilt aw eSlaCOs WN iii cr Finale Meera cinalmon Glide « Since MN Ae. ky 324 
HerticolturalGrops Reséatch Laboratoryit.i s/06 Baie ee «che es Seek sala shee Hagala OMe 270, 276-281 
Horecuiuraiiusects esearch MADOLatory. yee. aches eee hie Seve alets act Meee gael ean be 3.152316 
Firetree ELOVe Chm nertretet a tanto! fete nie aia anaedad ah NOE, aPebnisla whe qigleds al folaneiy Woe ey Wee 285 


551 


U.S. Department of Agriculture (USDA) (cont.) 


552 


Agricultural Research Service (ARS) (cont.) 


Indian Laboratory «00 01a ea eh AR a reece OC el tee pees 24 25,40 
Insect Attractants, Behavior, and Basic Biology Research Laboratory, 

Gainesville}, Flccc wey seek Pog in sien SOG Oe I, Sere ie es ea? ee 63, 66, 263, 303 
Insect: Biocontrol Laboratory (IBL) <4 \.c.:.2-1-)-e eer ere eee 34, 51, 55, 69, 149, 298, 304 
Insect Biology and Population Management Research Laboratory, Tifton,GA ...... 62-65, 288, 289 
Insect Enemies of Aquatic Weeds Laboratory, Gainesville, FL(IEAWL) ..................0.. 39 
Insect Identification and Beneficial Insect Introduction Institute (JIBIII) ................... 49-51 
Insect Identification and Parasite Introduction Research Section/Laboratory/ 

Branch, (TIP) tases eee ne 23-28, 36-39, 49, 50, 57, 73, 79-81, 148, 150 
Insect Neurobiology and Hormone Laboratory Save 3. = ee errant en 303 
Insect Pathology Laboratory (IPL), Beltsville, MD .. 34, 51, 55, 69, 262, 281, 289, 295, 297-306, 319 
Insect Pathology Pioneering Research Laboratory (IPPL), Beltsville, MD ...... 345354157722 1e 299 
Insect Pathology Research Unit (IPRU), Ithacay N'Y. cre aye eee eee ee 35, i/2a3e0 
Insect Pathology Unit, Moorestown, NJ (see also Insect Pathology Pioneering Research 

Laboratory) .i ds-art sage RR. SM no SERS Te ce ol cS Re ne eae ene 299, 315 
Insect. Physiology Laboratory. 24.9: 32th) POE ee ode ee ee 301, 303 


Insects Affecting Man and Animals Research Laboratory, Gainesville FL (see also Medical 
and Veteriniary Entomology Research Laboratory, and Insects Affecting Man Research 


Laboratory). .«h200. Pepa oss Se ee ee eR: eee 58, 64, 67, 283, 293, 295 
Insects Affecting Man Research Laboratory, Gainesville, FL (see also Insects Affecting 
Man and Animals Research Laboratory, Gainesville\EL)co 4, . Sec eee ae 263 
International Activities (LA) \..cme teak eee eee. Ch tice, 1 dee ee 47250513 AT iaao" 
International’ Programs Division (IPD)7. a. eee eee 44-47, 50, 261, 263 
International Research Programs, Office of, see Office of International Research Programs 
Jamie: Whitten DeltaStates Research Center/im< gaan. eee ee ee 81 
Japanese Beetle Laboratory, Moorestown, NJ.5< 3.4... -.. - mae eis eee ee 31353155 
Japanese: Beetle: Laboratory, Wooster, OH, <3. ee ee 315,316 
Knipling-Bushland U.S. Livestock Insects Research Laboratory, Kerrville, TX ............ 321-324 
Livestock Insects Laboratory (see also Knipling-Bushland U.S. Livestock Insects Research 
Laboratory) shastiis 32% 2 soy «Re a Oe Sete Cee Bee rae See eee ee 331 
Livestock Insects’ Research Laboratory; Lincoln) NE. -ane4i) teens fe cae. eee 294 
Medical and Veterinary Entomology Research Laboratory, Gainesville, FL.. 58, 64, 67, 283-287, 293 
Microbiology and Plant Pathology Laboratory, Beltsville, MD..................... Dita ave OF 
Mid-South ‘Area Office ts. wna. C2 ee. re ee ee ey) er ee 295 
Midwest Livestock Insects Research’ Umitieorn ate 60). 1 ae 8 eee, 64 
Mushrooniand Microbiology Investigations 2 acer mot ocivichsae tere rrteney set onan oie eae eee 40, 41 
Microbiology Groups /.ciide se Jeeh 2d own ae Re ek ee eee 40, 41, 92 
Mushroom Groupeisos « .tec.o.cdieiecrs ou nebo SMES SOOO ie eR os en ce 92 
National Biolopical:Control Program (NBCP), =. :...::0.)ee eee 48, 150, 152 
National Center for Agricultural Utilization Research (NCAUR), Peoria, IL (see also the 
Northern Regional Research Laboratory)i7 5 ea ee ee eee ee 289, 290 
National Program Staft.(NPS) a seasue en tee 44-51, 69, 74, 78, 83, 144, 150, 152, 153 261, 300 
Biological:Control, "Matrix Team” occ... 02-1 es ee ee 47, 48, 52, 73, 74, 142, 150 
National Program Leaderi(NPL)itiaenemeen ci ee ce eee 45, 73, 145, 150, 153 
for Biological Controlit.2. Gera. e. cane ae Petes. ee Sn ee 48, 69, 145, 150 
for insect taxonomy is)... (2k, Ae ea ek ee eee eee os 47, 48, 150 
for Pest Management Systenis. 22 1) tnt cet. cae Seer ee a eee 48, 150 
for plant pathologys:'. stearate hee 2 eR nos Pel bowed ronnier) oe 97 
for Weed Science 5... .% Fe cot. Aa erik eee eer Serre pean 145, 150, 153 
NationaliResearch Program(s) /s 24 cee Oia: ss oot Oe ee 44, 45, 47, 51, 73 
NO 20260: sip. dala 3, Sapte aaah A Baek aus idle acrg db ect A ee ee 45 
Nematology Investigations ja./na¢ Sh tO k...«! sas we Se a ee oe 33, 39, 40, 66, 91 
Nematology Laboratory: «25.5 0. susue:cencs ousuclle ccetede 1. eee a re ke eae 66, 91, 92, 262 
Northeast Plant, Soil and Water Laboratory; Orono, ME. 4.152 4. Jaa ee ee 296 


U.S. Department of Agriculture (USDA) (cont.) 
Agricultural Research Service (ARS) (cont.) 


Northern Grain Insects Research Laboratory (NGIRL), Brookings, SD................... Set Le 
Northern Plains Soil and Water Management Research Center ................0.000 eeu 58,079 
Northern Regional Research Laboratory (NRRL), Peoria, IL .................005. 2737 289; 292 
Office of International Research Programs (OIRP) .............. 47, 48, 50, 73, 77, 144, 150, 331 
Resi. Gantrol BauipmenvandiMenods Research: Unitwae ave. AOse Ae. RRA WR fdas se. 62 
Plant Disease Research. laboratory <crederick MD smut. kh ee at at he tee 88, 262 
BlantreshC ont OMB ranc law rarer Aaa ieis) ood ee ho. ork RRR sw 23 
Blan ErOteeliOng VISION rs end Wee ene aan tae Shee. AOS Lae eee Baty Sees 26MI2OR 1212 125, 126 
Methods Developmentisranchimmntea atari Tie. NU. ahem doe. 125 
Bollaweevl Methods Development Laboratory sc. seca. 5 2b na Ad Ro als 126 
Cerealiteati Beetle: Methods Developmentiaboratory: aa kto. wh) ate es 126 
Gerealiveat Beetle! Parasite (Rearing Maboratory sent avy ieied. Sake a eee ae 126 

Gypsy Moth Methods Development Laboratory .................... 126, 304, 306, 307 
HobokemiMethods. Developmentiaboratory a: 2e ek ae Se OH Se SRE. 126 
IniportediFire Ant: Methods Development Laboratory ....2/ 0.000. 0.245. 9200008 ons 126 
Emkasollwonmmiethods Development Laboratory va.) 92 29S ee A ce 126 

Pinkes ollwormeviotiniearingrackhitya- arn i.e aaeiae. 5 en ie eae RE hss 126 
WitchweediMethodsDevelopmentilaboratory wien foe se fe oS ee ee kee 126 
Metiousmpeveropimncnmecuipinent Centers 5 asa ae case nos nine ee cals MEE ae swe s 126 

Plane rOreceominstitute Sete tere SM ae oe ow La SSO e en 49, 51, 66, 69, 91, 93, 295 
Planer orection nescarciunit( be RU) slthacawNY tac. 4ct ass wn alag ee ade nt Meee 314, 315, 330 
PAC ae ANASTIOTES LAC RN ELAS he 5a x reas POD tas ARIA ANS LMR SMe os 23 
Plant Science and Water’Conservation Research Laboratory ................0000ceu cues 98, 148 
Pilantiscience rvision.ssee also |Crops..Research Division: .. Sn geass cee ca as 33, 39, 41, 44 
laniese ences nStitle ( Pol )ig, Marre, lant eenNe Rey ns ae os Ewen ee ee ord D15.66, 917.93 
PCa Ue NSCCESMMVEStISALIONS MOLONO VIL: amakitnn 4 to sot ernie aaa Nees. MERA, oe 262 
rat alcicrlea OOLAtOny mOlwF ant Feeding INSCCIS a4... oases f MEMS knees SRG hs a 81 
Range lanaunsectaoratory SOzemalie Mi. lie tery as nen cles ole Mec kets CA 58, 79, 311-313 
PAULO SOUL ere wna ae TMI Ne cs De cishks! was 4 HY Me tape om ns Mh eA on si 316 
Ranve ancaw cous; PaUOlatorvecnee aeeny oh 20 6 cones Matneh i le ode 2a 79, 90, 148 
Revional @ereanisease mesearcl Laboratory oc oii. os ae san seh etieks ee got 94, 95 
Revionaleastinemnesent ci abOlraonry mr ster eile titnun ltd « odes sw oe Male 4 Typ Aa i hs 98 
Research, Management Information System:(RMIS)e gis 92.2.0 005 0.0 See ee Eee 146, 163 
ETO MMINOIITINN CSCALCHELADON ALONY wee, et ces, sicily a's. Hue Ge eles Me PE es ca ag 294 
Borate ei Scasestoa Oral (SOL) wine wan an id fs teat. Sak ka +e kin RRR SA gw es 92-94 
South American Biological Control Laboratory (SABCL) ......................08-4 54, 77, 149 
Southeastern auiuancyuree: NUtesearch Laboratory. cco. sesame e hey ia wed ag Wel. wes « 57, 99 
Southern Field Crop Insects Management Laboratory (SFCIML)) .................... 57,025 82 
Southern Grain Insects Research Laboratory, Tifton,GA .................0005. 62, 65, 263, 288 
Solthetmltsechivianagement, Laboratory (SIML) see seatint ok ee ee ew ele oes o Daw a 57,81 
Sr UHLCIGIRIRE LATLTSE AT Ga MONI ct te nin ae ee leg Po incdig oy BSS ed DS PANS Mees. «y's sald B22 
Southern Weed Science Laboratory (SWSL), Stoneville, MS .................... 57, 81, 88, 263 
Special Plant Feeding Insect Quarantine Facility, Stoneville, MS .......... 0.0.00. c eee eens 263 
Sicueumetheseatcn CQuaranine Facility aise cb edsg ae daa Se Be Ae eh I 57, 81, 148 
Stored Product Insects Research Laboratory, Fresno, CA ........0... 6.0 eee eee ees 262, 276, 279 
Stored Products Insects Research and Development Laboratory, Savannah,GA ................ 63 
Stored Productsunsects Research Unit, Madison.W iors « 22). SRI ie Pec bn we 3 63 
Stored eroducrs avoratory, Madison; WI 24.45.0enoed Se ne es UO OT... 327,328 
Subtropical Agricultural Research Laboratory, Weslaco, TX ..............-.000-005- 63, 65, 324 
Suptropical Insects; Research Laboratory, Orlando, FLU) I.) G0 aes Bel Sa ee ee, 287, 288 
Systematic. botanyiand Mycology Laboratoryiqans sete. es ead a ca ces ee 66 
Systematic Botany, Mycology, and Nematology Laboratory (SBMNL) ................... 51, 66 
Systematic Entomology and Beneficial Insect Introduction Laboratory (SEBIIL) ............... 49 
Systematic Entomology Laboratory (SEL), Beltsville, MD .......... 49-51, 101, 148, 155, 262, 417 
BOCITICAIENGVISOrS a He «ore i ca RP Re ee es OPE RHE Ba AS50573, 714, 77 


553 


U.S. Department of Agriculture (USDA) (cont.) 


554 


Agricultural Research Service (ARS) (cont.) 


Tidewater Research Station,. Holland VA.) Sapa ee re ee er 4] 
Tobacco Research Laboratory), Oxford; NGtmn F-26 Gee Soe. eer tae eee aa 96, 263, 307 
Tree Fruit‘Reseatch Laboratory ..\..5% Jee Le ee le dere pee ee ener eran oF 
Tropical Fruitand Vegetable Research Laboratory: ames Vie ae een ee 63, 278 
U.S. Grain Marketing Research Laboratory (USGMRL), Manhattan, KS .................. 292, 293 
US: Plant; Soil,:and Nutrition Laboratory, fthacay NY os-08 nants tek i et eee eee eerie 314 
U.S: Vegetable.Laboratory; Charleston; SCuais no atectalee te vo cote ete eter S1653 iy 
Vegetable! arid Ornamentals Research Branch Wane aa. sires = ee ee chs ee Sarena 40 
Veterinary Toxicology and Entomology Research Laboratory .................0.00005 58, 63, 64 
Weeds Investigations. 1.4 iid ansee Le Reed, Se Rea. BEST RRA rie rents tone ae ee 39 
West. Coast:Parasite Receiving StationwAlbanys CA wr i.cicle nee neil eee nee eer 24525 
West Coast.Parasite: Receiving Stations Riverside CAvag one -cee er cnet eres oe 24, 25, 148 
Western Cotton Research Laboratory, Phoenix, AZ ................. 130; 1499262, 271) 272.279 
Western Insects Affecting Man and Animals Laboratory, Fresno, CA ................... 262, 295 
Western Regional Research Centerjeeeae. | Wines ae ete eee ee 78, 99, 149 
Plant. Protection'Research Unite sevaet Sere ae ee te 78 
Western Vegetable and Sugarbeet Investigations Laboratory ................... 29270, 27 lee 
Working Group on Natural Enemies of Insects, Weeds and Other Pests 
(WIGNE) 53s. kocsis sine nae Ge lendes cig) IP oe I ae 45, 47, 50-53, 74, 88, 260-263 
Coordinating Subgroup on Biological Control of Lygus spp. and Other Plant Bug Pests 
inthe, U:Sa4 cukyaiies. 1. oa CPR EE Bako) is ere ee 32 
Yakima:A cricultural-Research Laboratory , 2\j.5.apsc ene de a a 575298) 327, 415 


Animal and Plant Health Inspection Service (APHIS) ... 3, 4, 26, 44-46, 48, 49, 52-54, 56, 58-61, 70, 71, 


74-76, 78, 79, 84, 85, 88, 89, 102, 119-144, 147, 151-153, 155, 156, 
264, 266, 269, 272, 297, 304, 306, 307, 313, 330, 426, 430, 431, 466 


Biological Control. Laboratory, Mission; TX... 2.24, 2 eee aa ec. ee 121 
Biological Control/Philosophy i294 2.4 2... . cto ee he) a ee a 134 
Biotechnology, Biologics and Environmental Protection(BBEP)....................... 134, 135 
"Centers: of Excellence’: oe? s'yp5-dv ak Sain kl ike So oe Se 134, 143 
Gypsy" Moth: Parasite, Distribution Progratn “ic, nua: oie © «ie cena ee Ae One 59 a24 
ManagementsTeam (AMT) i 21a ite): na acinar ethan eo 134, 143 
Methods: Development: J rtejereniy area se oe we 120, 125-130 
Methods Development Centers (see also under ARS, Plant Protection Division) ........... 123, 126 
Brownsville, see Mission 
Hoboken preks detsed oe ate ise dais o$1s Sia tO Ln. Ce ee 126 
Mission.s:).5 saws o val SRG Rs yee CU ee eee LR FA 126-129 
OtiSe late: yews 2 esd is cee eres, MAE ane 126, 127, 129, 130, 304, 306 
PhoO@niX iced. as «vals BORD lo pediocin ae oe 126, 130 
Whitevilles«..3 s\ueyedl ees Ree Cet! Aileen he aie. see) pea 126, 128 
National Biological :Controlinstitute (NBCGD)ijavn. sseen ea teee 122, 130-136, 142-144, 157 
Bulletin; Board System apc ieare © 3 Mains veneer autho. -< ie Weel asc es fecal eek eae ne 135 
Customer:Advisory Panel (CAP) aise, acces ie ae cl ee eee 133, 144 
National Biological Control Service Institute (NBCSI), proposed ......................000. 132 
PinksBollworm Mass, Rearing Facility:.2:2 . os: Ge ainsi ane ee ee 70 


Plant Protection‘and Quarantine (PPQ) > 253. oes 26, 45, 53, 54, 56, 59, 60, 75, 78, 79, 


120-123, 126, 128-132, 138-142, 144, 266 


Biological Assessment and Taxonomic Support (BATS) ........... 0.0.00 cee eee ee 134, 135 
Biological,Control. Evaluation Report js so’... 1 a een eee see een: ee 131, 142 
Biological. Control:implementation Program s3e ea 5.). Heda ie itl 1215125 
Biological: Control. Operations (8 CO) sew tc eee aes ee eee 120-130, 134, 136-140 
Alfalfa Weevil Biological Control Programynci.. eek ee ee eee oie 122, 423 
Euonymus: Scale. Biological:Control Programia..o" as. umes uid aeeeeees 1257,130 
Mission Biological Control Laboratory/Mission BCO Laboratory .... 121, 123-126, 128-131 
Satellite laboratory for weeds, Bozeman, MT «.,i 02. . da esean 0d aveek 21s 125.124 

Niles: Biological Control, Caboratory.« 7a) ee ease eee L219 2255124, 126-131 


U.S. Department of Agriculture (USDA) (cont.) 
Animal and Plant Health Inspection Service (APHIS) (cont.) 
Plant Protection and Quarantine (PPQ) (cont.) 


INatIONalW Lepr aint ania usta Kamen tec ake a ale Aarne Ucar + tee tees 4 HONEA tas i 
Operanonavouppartis talbecen. wee lanes MUM eIe Se eae eR 121 
Program Planning and Development Staff (PPDS) .....................00005 121713 1,142 
SClencerand | ecnno logy gan eNnieen nA ere oh, Sandie tings Sh axis e aes lh pao a's He 1325143 
Assistant Secretary of Agriculture for Conservation, Research and Education .................... 102 
bioiogical contro: CoGrainating Council (BCC) il aie ructce chs Meteten eon, CS 152,51 5350007 
urea of Entomology: (BE Mea waaniau erate terete catia Gade ercoee 6-8, 11, 15, 296, 409-411, 416, 417, 440 
Bee Culture Paboratory, somerserandipeltsville>MD 5.4.2... 40-2. cR eee ae ee 296 
DiVISION OM Eco CUIUT Gare. ede MOP tre Pita cha Ms neh: AORN e aces 11, 296 
Division ovbee, Research enema Mme eRe Renita reroute ete. syn aal ay cE MOGI Ree. 296 
Division wor Cerealiand Porageunsects investigations ss ands ON NLe VER ae Rl PMS SN ae 8 
Division of Deciduous Fruit and Shade Tree Insects Investigations ................0000eeeeeee 8 
Division of Forest Insect Investigations (see also under BEPQ)...... 000000... 0000 0a ues 7, 8, 409 
Gypsy Moth Uaboratory, Melrose Highlands, MA... 0.29494 24 «eWeek Bes 7, 8, 409, 440 
Centrale uropeait ay cstisallousn arercm stews teieid ounce talent. bene isha eet eRe ace wate gies 8 
PUrOpeall Ome SOLen abOralorya mares etn as iincrat onlacate ee aay tO OMae mee alin. cs ables & 8 
Intermounaintstates bee (culture Field Labs Laramie: WY. (aches seri. relies so 4 3s. 296 
Bureau of Entomology and Plant Quarantine (BEPQ)............... 1520235259 2008101, 1257145. 
297, 396, 416, 424, 444 

Aicralidicn special MOUIDMent Center main mania care ineter.Lct 5) 1 SEER ety eee ay Mae ees 5 na 125 

Bee eulureiabOralory wOPalin Uae mena na. 658 J Saders ate ei he et MEE vires leas 324 

Beee unurer. mits avoOraory s Belsvilles ML) Yc tbh) nee che ote ee tot aa ee. one Deena 297 
ono! INVESH ations: DIVISION weet e+. ot males Seacaten os Ske Ria Oo fey ule cls hm a MANE! Os 3 15 
PVision OF Dee CUltlteae eae ee oe Ree bre ome ok Ne PST 18, 20 
DIvisionowoee cCuluire aud biciogical Conroy hi deueatees oo) dae neat sane. Mae Nba ay 18-20, 23 
POLO BICAlCOMLOLOeCtlON tran. eet trate tints tne Gite sXe eRe Sr gl age aaa IRE nee 23 
Beekcepinm and INSect. Patnology SeCUOM © ate. 6b eee 6 Cane enn Sty eee Oe 297 
Division one crealandrorace ausecis we ate. oc nite ee Pies ae ae Pe» LS 16, 18 
Division of Forest Insect Investigations, New Haven, CT (see also under BE) ................ 396 
Divisional Grergmiearasite, IMtCOdUCtION eic.ten wi ee Steevie eee ees ols Rts RN ciate alleen oe 15-21 
Asianiearasite Laboratory (APL) (ses.also under ARS) 94.5%; 52 ve eeas Ve. ee eae 16, 149 
European Parasite Laboratory (EPL) (see also under ARS) ..... S.11550 1 718921524527, 36.158 

SOUL MAINenical Parasite, L.ADOrAtOryian ay mths ae ace tte Scarana mec eRe eee ef ae eee, Vides 
Divisigd OMETUIGINSECtS Bae. aoe eR AL en ee hn cre Oe NE Leis Ue ead eee 3 16 
Division ommeece Detection.ang LdentificanOnummne 4 senna eh. ass Me. So oe we 23 
INSECT CAUONL OCHO er tmet Ret ere Atte las le Rpeyn. hacia s RUS Mea ae tc oetnas 3 23 

Foreign Parasite Introduction Station, (Moorestown, NJ) ....50n5.-.eak ua eel wine Ms. 18 
Siti ee OP ALON V es bes aroha er hs nts 2 hore Riches Wed MH Pll IAS NIUE occa) ea ace 16 
Japanese Beetle Laboratory, Moorestown, NJ (see also under ARS) ...........6. 0.000000, 20 
RISC UAL OD Ys WTAE epee ean tiratcter ns ey ort arin Eas ape atch ec UM DRM chia yaaa 20, 34 

DMMomres OWI RecelViNe OtallOl ay cere: | eee Ren tle a ees nla aes BEA es (CRN La Bee ees 16 
U.S. Agricultural Research Center (USDA), Beltsville, MD (see also BARC under ARS) ....... 297 
LES@entomolopical Laboratory (Moorestown; NJ) <...a 000% <a oh ose ewe wae s ves eee ees 16 
BUrcatrummeianit IDGQUSITY (DBPL) am cxiccedtet tants ida fide Bal Wel erally wie el eieie @ har geet ins 10, 12-14, 19, 22 
Pereamad morace C1Op Disease INVestizatiOns a)... ver ahs)se stinks pat wie aula ws ele sing Ss ae es ot Ze 
DIVISEENY OLIN COIALOLORV Merri 4 Sire MC Hie sels op Sakis ae etn F Vig O ME wre « LEN 3319721 
Nematology Investigations (see also under ARS Crops Protection Research Branch) ......... Lie i2 
Oiilice wat 4 eric (irals FeChUGlORY, {pnts at ahi et sc Sixt Hd aie coe ROAM aisle eae s WOW G alow nie a 10 
Orriceoh [nvestioauons INsrOrest, Pathology: i.) ai. jctatlejs a ao ese RIND Mabe is nel oe ls wee 13 
Soianc Periilizer Investigations: . fee a'vcc%.u nh bas oh 4 cle viele ’e Wisma hele ehla viale's see es ale 22 
Bureau of Plant Industry, Soils, & Agricultural Engineering (BPISAE) ................. Red boo ete ts) 
FOricuininal rons Research DIVISION cisc.ane geen histatins Wo teivve ites Mecle Riinle a HMM was ld as oA 

Pr a OlIE AOU AT ATSIC I etnias sree <inlalate sities de «else Pe nares Dera NelliGlmie saw ts 15, 416 


555 


U.S. Department of Agriculture (USDA) (cont.) 


556 


Combined Forest Pest Research and Development Program (CFRP) .............5.000 ee eue, 407, 418 
Douglas-fir Tussock Moth Accelerated Research and Development Program ................. 103 
Expanded Douglas-fir Tussock Moth Research and Application Program ............ 113, 435, 438 
Expanded Gypsy Moth Research and Application Program .................-. 103, 111, 418, 419 
Expanded Southern Pine Beetle Research and Applications Program (ESPBRAP) .... 103, 104, 109, 

402, 403, 407 
Gypsy Moth Accelerated) Research’ Programme sias a ke) ae ene en ee eee ee 417, 418 
Intensive Plot:System (IPS): siete Wi ncadicn ss Bet eee SROs SUNS eon 2 eee: 102, 104, 418 

Competitive Grants Program S®.4 shia Seas sc Nils aad cincdiakc cn enene bein ee 415 

Competitive Extension Service: iii Woo ci Baers ten tee mee ntanta it, pede lai gee een 4 

Cooperative Research (see also Cooperative State Research Service) ..... 024.45) 1) eee ee 46 

Cooperative State Research, Education and Extension Service (CSREES) ................. AXIS R32 


Cooperative State Research Service (CSRS) (see also Cooperative Research)... 4, 45, 46, 48, 52, 53, 102, 
122, 144, 151, 264, 278, 402 


Regional, Biological:Control. Projects wateicwie Sew ee Ti ks 4, 133 

Regional Research Projects). 22k . .anin.<-> «to Ra ate lee | ee ee ee ee 151 

Southern Regional Project. 136. ass : 2453x465 Je os cen 90 

Southern Regional Project*234i4 . scree ho ee Set ee 90 

Southern Regional: Project:240: £5). td ee ee 69 

"Directorate for Biological Control", proposed establishment’ {.54\...9.. pwen Ge ene eee ee 192 

Division of Entomology <scaran en Ash ny eed (cee Gs ck ee Se. ee 2 Be Pe ee 6, 44 

Division of Bee JResearch aijnq e156 dvs soo 00s eve 4 dasneenc, ANU Seee etal oe aie eee eae 296 

Economie: Research, Service (ERS), 2.2508. onsa couwis «<u 5: Ree ee 46, 127, 264 

Economics, Statistres, and CooperativesService =.= 24.01 Sane nen ae eee ee 61 

Environmental Quality Activities,Office:of@, ; x, inne cotta nee ee 45, 46, 264 

Work Group on Biological Pest Control Agents (WGBCA) ..................... 45, 52, 264, 265 

Subgroup on Introduction of Biological Control Agents (SIBCA) ....................000. a2 

Environmental Quality; Programifor’s:,%.4)..4-« «srs dais coy oad | ae 45 

Exterision'Service(ES) 45, 45. See eon ee eee ee. een: Bee 46, 48, 53, 122, 151, 264 

Inter-agency Advisory and Action Team (IAAT))..5.5... . camer. Oe ee le ce, ee ee 152 

Federal, Research)'see:alsovARS saieneh ae ee, See eee eee eee 46 

ForeigniAgricultural Service (FAS), 2 Geet oe ee oe en ee ee 47 

Forest Service (FS) ... 3, 4, 23, 45, 48, 59, 100-119, 122, 127, 151, 152, 154, 264, 288, 303, 307, 395-469 

Administration fan . (eR eee: EE ee eee ee ee 102 

CarsonNational ForestiNew Mexico 2... 4.2: ss a eee te atin 451 
Center for Biological Control of Northeastern Forest Insects and Diseases, Hamden, CT 

(see! also Forest Insect.and Disease Laboratory) een teenie ee ee 421, 422, 425 

Division of Forest Insect Research) (FIR) «...-. «.. 226s. sam Semen eee eee ee 406 

Forest ‘Experiment Stations’. ’..+ cn 157aa 8h ote Re eee ee 100, 410 

Intermountain Research Station (iN) aoe. «n. eee eee 1 eee 396, 441-443, 450, 451 

Missoula;;MTS See ete oe 4. eee. eet Beet eee 451 

Oaderiy UT Mais 5.0 48 boas sislncss etal ese ws acs Sees oe 450 

North Central Research:Station (NC;NCFES)_ . 7.2... suman ae 105, 415, 439, 452, 456, 457 

EastiLansing?! Miviney soa eon A oie ee eee eee 415, 452 

tp Paul, IMINe hora J opt). .c dao Ae RN 5 ee 456, 457 

Northeastern Forest Experiment Station (NE; NEFES) .............. 104, 105, 409, 416, 424, 

426, 428, 440, 445, 453 

DelawarenOH (a5 205.. See G RR A IE hes tech a iso nse Se Ie 431, 432 

Forest Insect and Disease Laboratory, Hamden, CT .................. 416, 419, 420, 425 

Branford, CTA, Paes ok ok hin eT ee eee 419 

Morgantown): WV 08 oe: 2el an on ces ee See 415 

Néw Havens ea apeias ieee omer, 416, 417, 419, 420, 424, 428, 429, 431, 450, 453 

Orono; ME:axs. ) Cee Oe eee ee a eres tg kB ote eel Se eee 445 

Pacific Northwest Research Station (PNW) ............ 105, 412, 433, 435, 442, 445, 446, 449 

insect pathology project’) Vial. ees Gs ws cx eek 436 

CorvallispOR Wi) Genre 2 eA Gee odie. calcu nhc aee scntik eau ice, ROC 2 436, 442, 452 


U.S. Department of Agriculture (USDA) (cont.) 
Forest Service (FS) (cont.) 
Forest Experiment Stations (cont.) 
Pacific Northwest Research Station (PNW) (cont.) 


AR ATATIC® 3) Rar MMII NRE CS db et 8 a ate ls eel ee a aw lh leis 445, 451 
POMEL a7icl AG) Raa ee MO Ec cl Gans sishi- a sod wsdacacace «nals anpactiemebetaln 435, 452, 454 
Pracilic SOUUIWESE INESedECN SLAUION (las W.) acd scciviin tk > dw o0<'o.0% ciel ore a oo veapnelaklctan 105, 412, 450 
Be Pa eR oA gsc a, a 's1 2% beni pits bedomaalh cal auuleomn muadveeabery 4 450, 452 
Rocky Mountain Forest and Range Experiment Station(RM) . 102, 105, 396, 404, 411, 412, 427 
PMTESTCCT EATEN IN IGS hoe Mt ol de Oe rhe er ne hee 404, 411, 412 
fafecaminver ie, IMB Say 2 PU oe ee oe re oe 411, 413 
IB EVOS lle OU es. Oe Pe 427 
|Log Oe) TINO Oe eG oS doar Ske ee we a ne en ee 412 
EGO ry en ae eles. Ges sa hw dow ao Sono ee Bs All; 412,413,427 
Southeastern Forest Experiment Station (SE) . . 2.26 wend. eure ss 409, 415, 416, 453, 455, 456 
STG VE LGr IN ame mae Rr HEM ooo ch 28 by aca8 DS andi bua & mymdodva di auaonRldore de «ae « 0 453 
TRA CTICU GHA Sia Sahn 3 en @ ob, ARO LSE SRR ec ee oe ea 416, 455, 457 
INGsCuL Cimon ialeicst al KoNG seater Cyt Eien ius sce bas 6 agar eeebi cane res 415, 416, 456 
Southern Forest Experiment Station (SO) ......... 105, 403, 406, 407, 409, 413, 414, 432, 438 
TEI EA OAPI Me PR mere ye Ses sts tag EES w 4/5 <5 ace od wheel ofebais GARONNE Bo: 409 
PAPUA ee Py hones ce oe ee a a er oe rr 432 
SEOREN TOM SL rma ee a Mia Ariss cc kia. sooty us aon «sc sh ayevamyieu ta Ronde eal Ae 9. « 413,414 
Forest Insect and Disease Laboratory, Hamden, CT (see also, Center for Biological Control 
Om NOTiMcAsterl MOLest INSCCESTanCDISCASES 5 9s kc oer S ctrl tae © Yaesu ais le 425 
Forestansect angusisease Laboratory, New Haven, CT .. 2.55 os anieneu Swe sie edu wind os 416 
Forest Insect and Disease Laboratory Field Station, Branford, CT .....................0005 419 
Porestunsect Laboratory, 4 DiquerquesNIM garters yet na sake BAPE exngs oes) Daves circ Wbiweas Ss 2 asa © 404 
Bereculasecta apo atoryy © Our Genes Lea i coals HE Rectal nigra Ga dks verte e's <9 2 397 
POPS StAMASC CER Y Otic Clits by Amr tem hee er eel gh ous 55 catca ahead Mash vf phe ees & ble a woe eae eaten aha § 409 
POLESE ESE OTICO | Mera ae Res rare te nics) Ge Gadel euseueadiere seule dl wittgisey dues kaa kee 100 
PoresernysOlop yi LabOraLory, DeltsVillen MID Sas bee mde at ors renee aires aA +. 0s fa nes 459 
Forest Products Laboratory (FPL), Madison, WI 22 os 2.4.0 ee be ise ee oalatle 100, 105, 462, 463 
BROT ESE SERVICE LO IMMERSE C seen Pieter em erence. chan (coo x'cia. wie i qe Aw wctioees Ria thens bh sees GSAT sa 435 
Potesiyc enrel, Binevinie, nical Alexandria LA co ee cen Fas op + OS aisles es b eleepbites Ws 5: 396 
Forestry Sciences Laboratory 
PASE MINS oa 5, as SRA hs Oe Te GP Oe Se eee eee gee ek rec ane ee eee eee 459 
Ce CHTETA Ole LTCC MCOUG MOLODY aah aie tea bie, Actes as aff es wb ys arin A= Pumaren’ heme ee 460 
orvallisn@ Ree aiee ee Ce ete ee ete a tS al? tun shades oe aihwm a 410, 411, 435-437, 460 
cell We Ere ne siete eb aa at Pe ech lady Sea nemnia os Fsdhl th reat yee os, anf a 426 
NWLOSGO Wa DL) eeeteMen nei, She hea eo ae ih dia wa an « eemuanemdbnne A charts oman IGYAS jnrssanesanwrepairihs 462 
Co ier He ir eee Ng et 0a), os een er alae pnaeda ps Brame MG THe RAeNN? x tad 400 
Viney lem Mr eee ee ote Ne ee Nes fa aed ioe See wala’ d 396, 404, 406, 409, 432 
S COTILLION MIP ee Onan ek a fear hore Se tah Gy caens anh a ores Wn Van eaeegneme mena 404 
Gypsy Moth Research and Development Program (GMRDP) ................. al leet 234224423 
Insect Pathology and Microbial Control Work: Unit oo. s nec eemie ns Hin nine whe emu aie 424, 425 
Iseeercaniies aGiIItVa MiaIien: CL tamacee a artaleg eee eda ola. © 4. heaps gare a, uhiogahaien swale sings 421, 422 
International Forestry 
ECO GAME OLE sin yor TORT AMIE ete ein lls Guo G0 sy Rare hia tigsita lod loeunia Sgeatigekyel levi dr 106, 454 
BESALC IGEN RIO ORESE LGA cater gs ReMi esta Beate an che OUR 6 palin is cape leTh guage deine regvyaen 2 407 
BPaTC ONSEN AN IAELA LE OL ES toe Ve tie ray te ere ke at ale steak Sool eieh a o's ese. ooo «eg Reming treatin 405 
“National Center tor korest. Health Management oye cccieataats aim wjeaaie i Rynareeiel stele « Gi slime te a 106 
INATIOTTAUROTEStEA CUINISErALION se cisus ome o ig ata ssot e 2s ciete aie 8 rand a eT Vie decane ad 100 
TATIOMA OLE SUsumene He eRe rete See @ 0 a ee ce a PRR he da Uapetn aha Senna IS etna Bn 101, 106 
National Steering Committee for Aerial Application of Pesticides Against Eastern 
CE LACORS eee eee atia of KU o rm oh as cc ss © sMeusdceinrieedecoh ete ieedeos BEB, sumndcenesy 430 
TEI ASICA uN ALON Al ROLeSUR nue re re iat eee clas eastside aS « 2 ageS¥h bagtatainns Bm Saleyucet 411 
PEISETLICASCOTOD ACOA ME TE ate ee ety es Cae ls Ws es See CE ees & © whatelayaaally cde NORE eons 450, 455 


357 


U.S. Department of Agriculture (USDA) (cont.) 
Forest Service (FS) (cont.) 


Programs’ and Legislation fim 5 oe ie oe Wace deans ooh oe perme ne e gieeeya ee ert ee 101 
Quarantine Laboratory, Ansonia, CT (see also, Center for Biological Control of 
Northeastern Forest Insects and Diseases) %) fase? a. vo a Mtoe ee gee ea oe 106, 423 
Regional Foresters iif. eee es ren see hea sco ones oe ee erect ta ee 101 
Regional Offices 2.0600 os Gre pe eee RN aida es pee einen nee coe ore ete Eacee tetera 105 
Intérmotiitain Region” oe se seas od Ae ee eg ee er 399, 401 
Northerii Region sc gee eed nee er Phe Sis ee tded aren gre ate it arate eet 427, 433, 441, 450 
Pacific-Sotthwest? oo oc 240 Sd id AER ASO Mt DIG COR Tee he ae eee eet ee 455 
Region: bight iy shee a cd eh ae ta PA Ob LLP AS Bae ei eae re ee 411, 442 
Region’ 6 AAs Py Rye) pa EArt aren et Patan the Ps a cick nt Meee en ne te 436, 441, 442 
Baculovirus Production Facility 72 225 Ae ewe a oad hae. ae ot eee nie cee 436, 437 
Region: 8 on hx Pee etn Ch recedes te eae a hole e Whats Salalle te aight nents eae ee 406 
Rocky Mountain :|Region (Region 2)°.25 99. c-2e ese cnc kee ae ey eee ee 433, 455 
Southern Region (Region’$)"% oa. 2 e525 052255 es oh ed An ales ct ee 455 
R=8)AshevillemNGO oj-ce9 asd GAR B0b SEE ee ode Le ee ee 455 
Southeastern Region 6) 3205 fo cneu Dasa SRE See Mae paeBee leo es eed ee 438 
Southwestern Region ws 20) na. ees ead. Na TS naan she roe ees eee an Ser ee eee eee 455 
Research 4 ech) Fe re he Phd BSAA ROT Sa BRAT ee 100, 101 
Forest Insect and Disease Research (FIDR) Se rct sans 27 ecaes ge woe eee 100, 101, 103-105, 438 
Forest Insect'Research mead fo a.nwee sod PW Pars Oi PERE See ee ee ee 100 
Forést ‘Disease Research ieee ast Se oe Ce Dre ee 100 
Research'and Development Effort’. ¢¢24.20. 2501 22s tee See eee ee ent nt ane ee 435 
State-and‘PrivatesPorestry eee ene ee eee nes eee 101, 423, 428, 433, 441, 450, 455 
Forest Health, see*also Forest'Pest Manasement. 4.500012. 1) ee eee 101, 104, 105, 106 
Forest Insectand. Disease Management (FIDM) =o: 1-3 ee noe se co) eke re 100 


Forest Pest Management (FPM), (see also Forest Health) .... 101, 105, 406, 411, 419, 423, 426, 
431, 436, 438, 441, 442, 454 


Appalachian Integrated Pest Management Project (AIPM) ....................2000- 431 

Baculovirus Production-Faciity; Corvallis, ORM. 2 ee ees ee eee 436, 437 

Station DirectorsPl £N205-5 3 ak Saree ene ec ee eae er tat Oa, Gree en 101 
Wasatch National Forest? UTtoak fas P eh oe ee ee er eas Ss PPS OR eee, 0 ee ane 401 
Washington Office(WO), 295 eae See aoe A eee se ah ieee eee 100, 101, 105, 442 
Western Spruce Budworm Operational Suppression: Project. 7.22.55. 4s++-- 00050802 oe eee 451 
Meacham Pilot Study *:: Se aga ee Ee PAR SAVARD ORS oA Boo See 451 

General Counsel Office oF (OGC)* soiree ie = ce rer ce ies ee eee ae ens 46, 264 
Integrated Pest Management Program for Bark Beetles and Diseases of Southern Pines ............. 105 
Interagency Biological Control Coordinating Committee (IBC*) .............. AS, 52,54, 122, 1519052 
Interagency CooperativerA sreementis "sais. os Seen at canes mente co eee ee 125 
IR-4 (interregional Cooperative research project), wane aa Syn he hones once cy ye ee 278 
National‘Agricultural ibrary,( NAL yates rae eae ce eee er ee 48, 297 
"National Biological Control Program" (NBCP), proposed (see also under ARS) .............. 150 9fa2 
Office of EnvironmentalQuality Activities({OEQO)" 27...) oot ae ee 45 
Office of International Cooperation and: Development (OICD) "7 3-2-2 +.-..+. «28.200 eee 46, 420 
Working-Groupan Forestry o:43s 8405004 fae Sete lay oes ea ata ay Gh On ee 420 
Pesticide:\Coordinator’ [447s £2) age Oe Bae i ed Sime Fels 3s Fiala tain were ek a hes Se eee 46 
Science and Education Administration (SEA) 22722 us se) ose eee ee, ee ee 46 
Technical Advisory Group (TAG) on Biological Control of Weeds........................ 75, 82,91 
Weed Comunittee: oxo S06 Sih se a Pe SO treat aa ie es ko ae 37 
Work Group on Biological Control Agents (WGBCA) (see also under USDA) ............. 45, 46, 151 
U:8. Department’of Defense fa eas. Ave yao ag tees Da ee A eee Nae weed ae eee eee 260 
U_S2 Department of Healtly Education-and) Welfareaaye + ase eve ters eters ele see me 260 
U.S.Department ‘of theinterior (USDI)P snes nice een et trey Ce aes ene 37, 46, 80, 155, 260 
Bureau of Land: Management mts iin Sear sie cae ee) eee ot ee, ee 79 
Bureau.of Indian*A fiairseaty Sane es. hs Wat ne ad Pn ee ke opt atc etre os ae ee 19 
Fish.and  Wildlife-Serviceta:% fe gine 1 eee ee Gk, cen te ave ee 83, 89 


558 


U.S. Department of the Interior (USDI) (cont.) 


Pe eOt ae ear CIVICE wane oie CRMM MeN Fkely tre Tuc oe og Bk ce ie tile alg 80, 149, 466 
U.S. Environmental Protection Agency (EPA) (see also registration, and tolerances in subject 
IVER) (eres es oe ees 2, 12, 35, 36, 45, 46, 49, 57, 64, 67, 68, 70, 88, 89, 91, 94, 102, 103, 105, 152, 
154, 159, 260, 278, 292, 297, 299, 310, 313, 320, 420, 424, 425, 435, 436, 438 
Us eoodtancorus ACMinisttation (FDA 4 uke she ikitle shee sass sules dug eaden eeu 36, 64, 297, 318 
Ae ETC OEIC mem nema tens is emer ne Tete Noe Re sh oi oN Witnla ony alle ws woe ans POIRIER oP 6 
ESUseathO Le CLIC UU CR em rune a Teeter eT Encl aie G & via nce alu e cw AcUR cobble apeiplobe alte lle ka 6 
SeROMMMLCNE AIK PACCIN AIK GLICO.) niet e EMME E, Rion e Ra CK's Glas ata’ satel ce ey ae Ree aie weil 427 
Pee CU TACAI LM SOL VICG> ree Avner Rr Scaled obi ae %s ik sb ale ace koe Goka oe be tee inten ee 285 
Pet ots Ke Cience ana LeCnnOlogy A RTeeMeNtr. ks... hia wins wae ele Sota ob eG 4 ae Oho eb 420 
eerie er CAGEINY Ol OCICNCe LOOIOSICANINSECULC TA oti shers sie wie dole cin Cee Wis eels bee be obo hee 56, 76 
RE aEIE UALS RTL VOLS ICY Meet Pa etter erie tae Met AUT APG. M05 15.16% tail c's. 55 waln "side fa ia Ms °@ Wodne! null tel biG eecge DE, plinde Wade 324 
V 
Misgimasrolviecunic Institute. and State University (VPI) ich. chloe eu dre no hs beh dau ws see blew are 38, 53 
DTOICanATstitUtemiStae Maree vee ee etacmes rime ee ere Me MSG, Lv cise ce edwle cs chalcw awe eM 6 ¥.dee 99 
Ww 
VB FE TIELIGS SY EA TUNA UF 0 aR ge Ait nr ee A 94, 324, 443 
SOR IEHINOLST POLTESt Hilt CHTIGl Ch Cal airan et ere hee eve wae 2 oes Ble es aise wbcleiase) iad aihime iia ke a antieteg ote 424 
Mleconcin, Departiient Of Natural Resources Rhinelander |... 4 fos eee ce ie ete pul hopes etme 450 
Working Group on the Biological Control of Weeds (joint USDA and USDI) .................. SW ee 
Gees Aik Pm eer ee Cin er Fhe, te Rate gtat toh, eaiais Cee Viale SN A'S ki ES aie dee fp beat are ed 106, 454 
RCAC COMPANY Ferrera an Fre ORE see eae ec Gt ata ee hee Fars hl eal Hoe AhaMaeR Mg eal Goel as»? oes lain, igs relay Ap 94 
Y 
Ne METER CACY Mmm RT Tie ce Pe nm Pate Strands, AN Og Be Gacincicalse bated ones Wie &, Binlnp ae ai Weis Sooty ¥ pwllevadars evans ks 424 


S59 


SUBJECT INDEX 
Compiled by S. M. Braxton 


A 
abiotic. factors/COMPONENES sos ss tie cie ee > pom cee 2 oe ast sett ceatan ore eet Nee eee nue ge 455 
acaricide(S) toasts aig an 6.9 cnsoy use see eecieb ns ape earls use ecaent Rel aol a ERO aN AOR aye ana tt te ee arene 283 
acetaldehyde? oa ace ace coughs airplane te oer ane tonne Sa gots ales. ot sient ue ns ce nce <2 66 
acetate SClECEON cc. acc ae ssi wae gee cae Fyn ON ats dine eke WUE wba crete tate arte ols ee Nees ee ee 300 
activity 
OE Bt digs arece okt Sead eesenconag an as pd eosha sodas Beane eg Rca oan eee 415, 429, 430, 432 
Pay GAYA | hcl =5 oan ae aaa RUNES OMAN: rain on, NVR PLA be A So did hoon Pete eS Avot Let rs ductyoy 425, 436 
ACVUVAINS, 5 seh cey aia ts ccs Gaae cere am oe eine ear ay aes toa ed cee Ret ore 70, 159, 271, 272, 308,319,429 
aerial detection (see, also Momitoring i.) ac. ose ie oid © ete oases eee eee eer ee eee ee 406 
aerial Spraying/appliCaulOn Ai cons oak tas cites cua) oc ca eee 417, 425, 429-431, 436, 446, 450, 455 
OL BU oe acta: «Rosch eae 2 oe US cas oe he hae re tooo RE ea ee Ran yt cee ae eee re 429-431, 450, 451 
ulira-lOW=VOlUITE “Wea wa toes) a sce ee fede e meaner ein meet oer oe RR erating ce a er 451 
Of Vital AQents occ: trees erste ok iy visun Phas sy shy ere caste cast ace cee Pet ne 425, 436 
Africanized honey bee; see also honey been taxonomic index ee see eee eee 297, 324 
agolutiniating Substances me ac. ese Sak cs oP ots eens eaten hae ce ee 273 
Toy a4 180) 1 ia at roe inte ly ae apai ra, kad Rall ie i elon i ead es Stents AL AS amet aus Gyo can 0» 403, 414 
Agricultural Trade, Development, and Assistance Act of 1954 (P.L. 480) .......... 0.00. ce cece ee eee Zo 
AQTOECOSYSLEMS 5.0 oo ose whee rete aie einer esauas aise Oe Ser ec eeMneRE Fore ree Rae ene at nee 137 
ALOT IN sein tse oigses, cis eos we. RGeres aS Mah eo Ree hs TET he Os RRM “oh Sa steer Phere oh eae a 413 
alginate DOU cc c.c ce pole» sare nyt e eae oe one A nT rae eee ho tc ae ee ee 94 
alkali 
liberation, techniques. oi. oe Ss si aie centre eta it gos I nt Ae ae zal 
LC 101 1 | aa RPE ARR Hae li iC MMi at ie wel Aue Mong rm et Bula re 8 ands, GPSS aus oo. sit 
All-American Catial, 2. rs. scans sic tecet oo RENEE cee Paneer Get eens nC ae Aah oe en er 128 
allelopathy, plant: sion arya. x ars asl «teks ovens et al gm ae ee aM te Peete writ ee ee a 164 
AMINO: ACIG TANSPOLE sno sca test gs Mate tou ist on aeoteiee rare ere eee tee ee nc 431 
AMMONIA Ys. aoe viens, ev bo = Loh tish sa peecaloaas, Woarale lacs” svat rs, sicue eirs met au eek ke etna oes ee ee 96 
ammonium nitrate (NH NOs) oe ocntee 1 ee siren ated tuere Cree cae cep mee a cael Sere ee a 464 
ant(s) 
foliage-foraging’ vc. se 6 os Sake wv mts eae sacle ee NE tee te ee 434, 450 
PEEDACEOUS. cos 27m ores tah gases os ena's. ery oath eons 3 cures ale oe Meneses ee de ene eee eee 436, 449, 450 
antagonist(s), antagonism .............. 1, 2, 13, 14, 22, 40, 52, 58, 93-99, 105, 116-118, 455-459, 464, 465 
DACtErial Sipe ns cco. oe 'u le atte cate as etatie Nozindar oon lace accents non aeyene ee over ee a Re So Ac ce 457 
fumgal” Meier «ois las wag Mamie Riva ga 8 9 Aes aR R UE Cee heer cas aye cetee PORN ce ee Rete UA el ee ae 459 
microbial 3. a2. 55 anus due vate s ose oieaes ca te cutee Steet ee. arr en make Pe nia wre ee ee 99, 164 
NEMATOME. ae accuse oareacdn ie Mare hand aee ie Seah tenn ren tenet ee a a 13, 40, 52, 58 
Of plant pathogens... %51 cess nae geen eect a ret ee eee 14, 41, 52, 58, 93-96, 98, 99 
of wood-decay MNGi”. sc scuis ousew sino aes acta eae eee ee a ee 456, 464, 465 
of tree/forést Pathogens 5a. xe csv ote eee ee ee he en et te te 455, 457 
antibacterial substances oo) ojocs.0rs sjcceses sue aye ge Wve es me eee as, nee ae ee 274 
antibiotic(s), see also resistance ........... 95-97, 99, 273, 274, 297, 320, 321, 328, 329, 457, 459, 463, 464 
peptidyl pyrimidine... c's «eon. cm © ha a ane oe eee cea yee ne 463 
ANIGESSICAME oie ose ec ggee wien nosle ad) i vn ow Mae Hoon Steen aes een eg er 452 
ANTE VADOTAM co ay ang, ao araneie ss nies shige oa NG RR TE Oran Ot heen ee ee re 429 
antimicrobial agents 55.5 ve = sss oat oo sete eee red conte Ua 128, 273, 274, 318, 457 


560 


UTEP RGIS: CONC oo ye rr 213 


ae cE TE NF ooh aia sagt nilenims2upirn a ws laors nian Sik.) Mca dbauectoedus Go 6)éa 40 pgm et os 403 
Bee ert Cree POE SO A RRR Pei es des sks ms ed an ssn G4 aH ae wD ein ee Lees 36, 281 
arthropod(s) 
PRU OOD NAG OUGME i AN CRIN EAN Gee SMR ES 2 Bi oin! oes x. = 4: Gilaght¥igers ings iad hace, nuda dues bes coon al oles 416, 423 
FOP AC OUR mute tan, aR Ir RE OW foe Sect pie Gis nee rie gop ah epee ene VR Se Hn 164, 423 
STUNT E TENSIVE cree, oy BC EI AE ie en oe ke re eee eet eee 434, 440 


predaceous, see predators 
artificial diets/synthetic diets .... 30, 32, 33, 35, 65, 69, 127, 128, 130, 271, 274, 281, 306, 318, 320, 437, 452 


OSUIIESIS TS PRS TR Es ee I 274 
Belimctamcoraliination.( Wit MISECT DALNOGENS) ic ies ves cc pe oc ne kee ad end Hw eps teh 6 wate 273, 281 
ema tibeslee (OOTLe Cue meme me ene Aa RT Emm fer kids cle Gl fp syain' 6 BRS « 2 diate ple Bb Gle Ged ae eueed 402 
BDC TAINS COCK AILS nee ENE ty tee Sct me Ed 5 (odie Ss eG Re ehatbs sl¥e se iayel Wa Sie, # yen. eie4 w oie Aaagegune ee agen de 449 
BeOS CUICEAC (OSI OM rater Wels Mi Na se PN Aa nee gC SEB acm diene pu'h. Hw Bcd oth gs bane sole sinter a 105 
See EAN eR ti eye eee aca Oa a sil sah a 6 96 lola yah tea Rate a cc Lacing prea sd se caren, S0n ohhh 322 
LCE nti meee ee A ee eI OTM Baars aha sha) fF al'etiecd oie auphe Ghbia G4 3 ese vin ere Boa Wiaveee oon wale 25, 26, 400-402 
augmentation, see biological control, augmentative/augmentation and release(s), augmentative 
TIGRIS ses EG rile tee tsa See ea en rake a 320 
BEIORGetTIMALLOnO MMI SOCl DALNOVENS a cist iat phen ct ed ei Faie oe y ashes hss sbeknee os op chum piace who tes T9S5:277 
eNOS UC i Rein eI se eA eRe a og alc ana Re sic Mass tb Bon, jah w suas Gls aay 323 
ARVO TAVCUN meee Pen ne SEMI tN eof EM ass 6 ois idole lita onde seis Fe oe boats old 4 vise so oh wales Fw 455 
B 
SPIES ETS 2 nty eh grass LE is ilies Sse don ce 307 
BUELL A ME AES 9 ioe ins se 31, 33, 34, 36, 40, 90-92, 94-98, 272-274, 287, 289, 290, 293, 296, 297, 299, 305, 

309, 310, 312, 315, 316, 323, 324, 328, 331, 428, 431, 450, 452, 457, 458, 465 

TERE EPSENASCR gad BSG op eet Wiel Ai ts RR tea Aare ee er one 118, 457 

SAUD ACCC TCM Re ery ier i a) Fh cae ek 2 alg micwellh eld Wide ha aac am 0 287, 290, 300 

STEN i Peron Oe eee ee ei RN no enue as ap wae oad aeivie Sa ceiite «ae coke, ae 96-98 

Te ACRES Oty SCM EN tee Mees er DN te art sgn ence eghyouss oF ave Gt, p dd due Saha oo Meepncte ahs 92 

GEE ee A Sek Gee indie ean Gis etl Gig GUM DI Gal elds deh + 60s 9/n oi So Pibeiae 90 

BAO ETS) LOL Z FL me eR ee Ree ea ahah Ries icanhe ced. 6 sR wis) Gg te dha Am nisl ¥ ne aan ode ectnltere 457 
OS RGTORNERTS “il Singtel Ses Si50h05 Ses BM cco ad St ar an SP ae oF 
Be Ca RSE Gs My ae ote rR ds Pw isc te os eu heeds eaten ned Aeigigrrdaapvicknialn nual minne's Puokidie 35750 

ASS AVEDEGCCLUILC SENET et arr MN ar TO PIER, ss sia ne 2s ved ees alana cana a ene 36 

REIC AOU OMe Ai ew, Mia ne ke be. sete oss isle dog deg ss Dea de Aiea wale Owe wine ae 36 
BE Att VME eee cate cil casa Pe UES oe Sieh ihe GS EL 5 eyo) octg Sud. is, cont dni tay duh ap we, pon 400, 402 
ra A ra Pe eet gee tae. oye ca heid ve od a ie s,s Ths Dp elw ob 8S, eames ‘aca dkepale 273-275 
behavior (see also evolution, behavioral) ..................4-- 396, 398, 399, 402, 405, 413, 417-419, 448 

CANO ED ah es SUS SRR AM pe BE OER EN ee en ee Cra ee 412, 413 

TENG ae dba 0 0 p85 UR BRA Sent gO ee a ae er 408, 449 

Ree tiom TT BONEN CCC Mr eee nn eile net ita sis suis a pied kei? adi Wye a Se KA a espe ns GA sept os 215 

ERE OOC Vali Gilt wr mere un ea Edo gtk ate ies eter c tusla cite alee Ger thn, She 204d, syaeh aaa nese cn 422 

Beal ee PE dn te RE Luar ated fe eoteina y te balance aw glacehe sales ws ewes 62, 65, 129, 408, 411, 413 
PPR ECSUANALVSisitseCsalSO;GOSt:DCTICLIOS, Goda peciain emis Ris ie Be vis elo eh aoe. o le wpe one FpopepeeeienmenssY 145, 146 
ae eae ye eM ae tn ove tu nicl Diptn cise ao .9d 54 vo de 82 6 oa wal note » halagumans 326 
ae ANC CI I Fo heap ssn plies ow fuels «10d gdhate dn massa ood Pobicbone ae Alem ys, Wma Moy oe 307 
eR ARSC YACU AES a Bar PT che CEI bp, een nisl ee) Sis = Raphi Sintelrhars ebotbeha lied Gaul 102, 104, 442 
BeeeMearr Tr ttn a oi sx lg ewido acennie card Mes ansaay hanno 103, 107, 113, 436-438 

Cab enls ales C mene re eect la a cs che enh ihedeidio tide Beli Aap die. ony cei’, Wee. ca ade hha cas 436 
biodiversity (see also diversity) 

TARVER TONS MPR PRE, 8 SRN i Ad Sasknie h & Gsth scape «dda eine EUbRs oe oes acho Aig 458, 460, 462 


561 


biological control 
augmentative/augmentation, see also releases, augmentative ...... 9, 10, 18, 19, 25, 29, 32, 45, 48, 56-58, 
60-66, 81, 93, 103, 105, 106, 110, 111, 120, 122, 123, 132, 
146-149, 156, 165, 278, 316, 400, 401, 408, 419, 423, 434, 446 
classical (CBC), see also regulation, safety...... 6, 9, 10, 15, 18, 23, 24, 28, 29, 42, 44-46, 48-53, 57, 58, 
63, 72-75, 81, 83, 87, 88, 106, 121, 145-158, 161-163, 165 
by conservation, see conservation of natural enemies 


Gost OF 3. cco the te ces Stale eas BAe cele ann de ee a ek aire Sau gtas S a er ee cto ter seen 146, 153 
commercial (see also commercial formulations, commercial production, commercial shipments) ...... 135 
documentation Of 7 oo. G2Gctee ce dente ee Sas ee eee ee 26; 46, 51953758) 107 IZ sues 
definition Of ood he ee he ee eae Deon ete eet ag rec cee erences tee a ne eee 1, 48, 96 
finding fore) cs5.06 fad Ey ae is he Satie ag oe tar emg oes Peo ee 40 
th preenhOuUses snucatee son « pesca ete tae ore Were ge geet cihin ctakceraae. a one once oh to eea meee 56, 62, 89, 94 
policy.and implementation [aii a-. 50: secre eine eee nee nae eee 131-134 
Biological Control Centennial Celebration” 9). 53.0 2 scce ce ee lk oe eee re 132, 143 
BIONOMICS rat ece o de ok a Peete Ue au ate odlagin: ¢ peltchelon: erie oy! ea enone tees te atte este tte sac eee 397, 410 
biopesticide(s) Wife... csi fe cn same camel ee wm eters ape Fee Ue aes cart ee emma ae 287 
biorational pesticides. 5.0.7.0 Aa ttra es cn cee sree oahe aiele nein © ps stkele hie oie ocr ae a a ee er 298 
biosafety of recombinant DNA technology 25 25.27% ae ceo one te tie see ne heen hl ee ee 322 
biotechnology (see also genetic engineering and transgenic) ..................-. 48, 78, 149, 303, 426, 451 
biOtypes Reds krrths tame et ee tle P tceete tte muna eee ait ne atay ase rece catel me Ariens one ee 423 
Birds wean Aiea hunter. Seren ee ee hos ke 101, 308, 396, 400, 413, 434, 436, 439, 444, 446-449, 463, 466 
borers 
beetle as Ue iewdns Lo eee ieiacds chokes & Mes aeons tot Sea eta ashen he em he tape wee aaa 6 Naar ee ee 101 
hardwood were os ee ce es ae ests cia ates ea Ate atthe Lace tod Gad woes eee cen aay eG Nee ee 102, 413 
TOOU Seki hess geste chines « ERR RRS GBs ce Gua oa mi ine eto ora eee Let ne ene ins teas ee 413, 414 
SOO the crea eee oe ET ey a wu ego eneae aii trer Rees CE eee cu esceee tee ae eee 110, 409-412 
truttkon, cetera era eek ie ere eas eee ee ce oN Se eRe Sects EN aN ee 409, 413 
WOOT Ses LN ihe cake Geteute ih san 4 ue chao tt tee cAI Guede tyr tee elented sala Cartes ee 278 
[Bas g (ee: 101 16 ONAN ae es a Bara a ard, eR A tee A A cc i erly Beda a td! BA IE RPE Rar or Co T1807 
Bora et ire Ge Pra 2 as 8S a eek fare ne Re oe 326 
bovine fecal mediuny 045 N68 Ue Meee eatin eves een ORECCe tao chr Mera ea Ut nies eee ee 322,20 
bran ‘preparations iV Vie ae oe ce nee ete ace ese ene eens cet ce a eet Rt elon oe ern rege 94 
Bt (see also Bacillus thuringiensis in taxonomic index)....... 34, 101-103, 105-107, 110-113, 115, 116, 118, 


147, 159, 272, 284, 285, 290-293, 295, 299, 300, 308, 309, 
317-324, 414, 415, 419, 420, 424, 425, 427-433, 438, 450-452 
application methods/technologies ... 158, 159, 272, 284, 290-292, 295, 299, 308, 316, 427, 429, 431, 450 


application: timing pers we cereus weer cat ches tates ro othe cette eel a ee 276, 427 
crystal proteins» inseciiciaal (ICP) ir. we vem naa etenr eee eee 71, 159, 293, 322-324, 414, 431 
CTY PIOteINs SEP he ites, 5 ake, ioral ass th ze on oe ne paies Gils cel on el ce ease eae ES ea ec ee eae 431 
CTV LAER EOS sate Sa va Sheer ee rr rt es cpt oe 432 
CrylITA toxin 785 02 etree ie ek ee eter On ea nore Te asd ee te eee 414, 415 
effect-on parasites =. ile Gf ows ah weet a sate satay ciel ala ele oer, Usenet ne™, Gee tees Oy me eee 420, 430 
endotoxins 
SneMMOLOKaN 2/5 heen ate ers tre alee mera eee 292, 293, 299, 300, 320; 322, 4314320 4an 
CXOLOXINS Poet Psi sla tele ein wate ares tno RES ete tel arate ee yt ete een inc ale eee Spa! 
B-exotoxin' 07" Gate eas elas steko takin ane teal) ee tree a tare ss eee eee 321, 322, 430 
food additive for livestock pests=.423% a. ace oie me tae Sera tert aere oe Laan enn 159 
guidelines for‘operational use of 3. oe wc ae lee es oe ee ee ae ce 451 
INSECTICIDES 8 pi caat eis et saul wie tte ce att ey ts ahr ed rr 415 
insecticidal proteins i Vly: inle oo. etcy satavere weet cies ane ee ee 300, 432 
Solation OF eres 87 oe eh teats why lees ane ane eee edn ce et 300 
parasporal inclusion bodies/parasporal crystalsiiia 25... cee ee eee 36, 293, 300 
Primary U.S, Reference Standard for 9 aa ccc eo saree re ee 320 
PIOCOKIN yee Gia wislateaere bese Shite bce oy 80 uate |oaie tema ati aR Per Miah ca ve A 293, 431, 432 
serotypes Ss Jo eelle elas a ol iava: Phatraln le ua: ene a: bsatare: ssteaetn ts pettenets aie ete tele age) ee ee ot een 300, 429 
SHTAINS Oi. ccedidatn on fncate pe oka te ie cena ee ere 97, 292, 300, 320-323, 414, 429-431, 450, 451 


562 


Bti, see also Bacillus thuringiensis israeliensis in taxonomic index ................. 284, 285, 295, 322-324 


Beet Seta COLLIG | MnreerwI eM a ROMEC ICUS LEN), gy Foca eee a dict d wedi tio ke WS Vode wl ewe Bw Eb ge we 461 
G 
eT 2 1 Ps. RI eG ae ee eee oe eee 105, 107, 117, 456-458 
uae S000 eS 1K) eM oN ey hela Gis ivy Gig aur piel. aim,o b Whb 4 vee ¢ boas aoc wie aw eiuie' oe hye eles 397 
CORT | lovato ales SAGER ode GONG Oe a TAI 5S9 23269 3271 
GAs ae Sere in Ee POR LE Be acc gh eb da ose a diie tym 8, 4bad o & oye Snipa Wal emepaauameaAe 6 450 
SEV ATED ido SBR EN, EEE, OVE TE ON OE GS See ne er eT 326 
Gann Oneal OCArOIe remain en eon ter ee 2 tl RA A oe ile ad ae RM us Be aie 460 
SANT SCAT ACAIC) XC COPE Me RE Re PR errare PN tres cn ses Wie aka in lehselaye ig Bln’ Sais hv Vie Sigs oie 4s ad wea 297 
SERIE TOT PESO TOE Gee Bein opie ler lg «i dad eof ee Wee eee te ne ae eee ae D3 
Cal Sm Men IRR cst ees Payette ey eee UG ittrs urate) Shin was Ais Gre! ak Avaiesiie! Wale oy ues gtboyleuone. @ SMe d wikes a tho een bet 323 
CVA oes oo See os eT 3 eis SR late Fk an, er rh rn 64, 84, 321, 322 
GASTROTSLTIES | Bikes Pe bee BG ce 2M SLAG UEUe ey Ac Bn rh ge Pe eae en 457 
cellcuitune/cell.lines (see.also tissue culture) cia. c ces ce ce ee ne eae 36, 69-71, 112, 158, 270, 271, 282, 
293, 301-304, 310, 311, 426, 427 
FLCC eI tn Pg mero, Wer Meat tin oe Ua BAe Si crng oatlscs i's 9 se oLamgeimie could wath eeieina dete 0, 0 Ades 301, 302 
Gea UNO LSU LS taIiGOS eae r ere Wie aarp leigh) wary yeaa auc casi ebeadaeuncadier ota bse meee 300 


cereal crops 
chemical control, see also insecticides, pesticides ... 23, 28, 31, 32, 40, 41, 102, 105, 107, 122, 126, 135, 272, 
275, 278, 282, 295, 308, 309, 316, 319, 327, 330, 399, 400, 

406, 407, 413, 414, 424, 425, 428, 438, 442, 451, 453 


Bae Te AUNT CS Varner nes Rae et ea RM Hct Hc ssichas Jl eH < Guaist ae Wied ale Bim Mhie ol Slee wa Vapl aun 286 
ie a PR a eet ee EN eer 2. ais ooo lei «ies ot levees Gos oie hurlers o°si9 * dude Ba llakxe 311 
CUED RCS EET ENTS = agen Lae, ih nse et en eer. 463 
ST SEs eh ete eee note il ik hk GSES OAL y.6 oa oeneae ER abe’ 310, 429, 450, 457 
earn steer Otd 21) Is SEC ee re ema eh ie he nial NIE LaG io tonsue will ® a ap tusin'e Wbaeawcn sol xpe Pucca 429 
AN LAIDG MPP ap eee FS Se ee ohh TNA el Ba Pa Bal Yl a he tld ce anata os h Qaeieicargls ac aca dadansie ayers 413 
EOE CIOL OC Al DONS Mr rater i CAEN is ov kei aye sooue a heal ous! Sycinyh A womlson f <Medlon,. ace. aavodecn tes 417 
Pept Eien GCM Or OCH IOLICCE cepa ge AI Rts eet sey aus hate inieie es srs Sie a le aja ashen ede shana ae 321 
sO) aera ree ents tA PEL Pes Z tte ice 9 Sedan ce iy chs atin Mol fo, Bs wale \cisid “o? ahallda my capa pr a ind Ses 323 
RRS CEST AGUTCC 5 mney ie RU hs 6 cc tS ciniins a ln diets Mila wi Bovine <lapigy GBid so 4 eid bee was 410, 411 
DU RTS a) oN) aeRO ch Oe ORO CE NCL ee POR MERET FM. ot ag Oe ee 321 
classical biological control (CBC), see biological control, classical 
clearcut/clearcutting 
A a eR ae cree Whee Peg Ed Nagar ah ei eh. AST wig 9.16 Be ree eee) dd val tu Son. pw lls, «oils 448 
Petree OD ANPMIIME Pte ree een te teete a es afi adeno St. hsp. 6 sch cause ut g's’ spots Valle, sae aahun ag 460 
AON POS Harr eR iggy Giada's «ste ee 4's Sek’ 4a '5 ces 293, 301, 310, 316, 322-324 
By Ae MMS Re en te ay 8 rei tae Od eles east ehahaeie Fins ws nine sbergee eden dr hueulioge pneu 272 
esc) EI el Seen errr at anise caste nieve > alisha meats ghee wuks) dltgnr ims Mgn eg taidayene ewe 461 
CL GUTSSEN TESTER US UG RRS ee ed pean ee ee ee ree Aare 125 
POM atONer pee fees gins Wks 6a wa ese as 291, 294, 301, 315, 397, 398, 414, 421, 423, 454, 460, 463-465 
ol ecpetata MEST TETIRT ODE oy eR Necro OC aa 457, 464, 465 
“ORES 4 Si SSSR TIRES RNG Sie Rarer cine ttc coarse ne ara Pee ee 306 
commercial formulations/preparations 
GES CTL MEI UIGTEFISIS (IL) eo tt pee pests <9 fiche ache depe, cut obs shiny shenmrtn nye nnidi sian es alnteedie. « 428, 429, 450 
Geet OE Ce eR tne EN ed Sre 2 Td phgith «0 ef Facts) oh et ase ems Swi ash oy ie MN Ra 464 
Pemmevelannanvest(OMCdID le TMISHTOOMS ) tet aiid are hie «6 eh ate no. ovriaie, woe atta Sax bowed soko cle ae 462 
commercial production 
POO a AP MTN totais, Os nro oun hed Pia heey la Nis aan neal aaah ans 3 0 sag gray 289 
Bs Fa Us (HPINCLCMSIS (BL) cress oats poe els eae ae a esis 34, 158, 291, 308, 320, 321, 428-430, 450 
Pee aiI IOs IEAISE SMES ool ioe cee ch scl ve oe le Fae aoe oR pe, Sega do 36, 158-159, 288, 302, 303, 308 
PSAING CMI Ee eee ral See Io's cg, vines. ck eta dW of Glace tien oils beta tihe sata Rvminde troll at ye 3 ae 325, 326, 328 
“ofl sei WATTS CATT LT earnteya FED GE poten gerotuar stare a Pee CLEP Ira pen Aen ere) Aa ae 302, 303 
Bee eNO TAC AV AU Mate ye ce ye Pir cle Ayaan carve ales) faye liy a)ia/s tune ot ng hth ape laa byes we og d 202 
Seah Tate MRED ee se ars cy 0 nig Ao) oe are wate avai ofc lm eythane olen ndad wield cartel labial a 287, 464 


563 


Ol nematodes . c; eo scs a els © ap ow 2 woe Foie 5 eae sor ae nrc ee eet Oe eg 33. 278,279, 267 


Of parasites’ ’.\s DE AWE. WR Te OR a cata ane ON Is Oe ni eee 446 

of Pisolithus tinctorius (Pt) oc ccc5 + osm «1a cee ee ete ete eet ne IA et Rl Rene ea eee a 460 

Of VITUSES nhc. ck Bad see ie oe ee > eres een een 288, 303,306, 308,310, 311,3138,3195425 
commercial shipments of natural enemies 27... 6). ef Pay ota als iets GP pete eaten ORNs 154 
Competition |. csenca is) susie oe Seem are co en ay CRnO Inte Peale tei Beene een eae 41, 401, 402, 427, 463 

INLEPSPSCHALC A AU. DR ee Tee EAs Pe ace oa ete naa arene eae 401, 402 

HPASPOCI FIC «,  evcgscravesavencracwrere vi cnere vary ghee sales 5 ietoee pki Ce fe cece CeO aR ge este ee ee 427 
competitor(s) 

GE tree pathogens’ so. coreg Sie ns dis uctieonsicin waren tage ua tole ee he ls he Re en i er cee 455 
COMCEATTIONIES AG os coves uaabecyic endive ery aly “esto vcr a RG IU ane baie ven EA sts eS sek TO et eRe r29 
Conservation of natural enemies. .n..- 1 ese nies eae reeee ne 9, 10, 19, 29, 32, 45, 48, 60, 61, 66, 106, 446 
Cooperative Research Agreements <0 iver. co arses arte usa tebe Peto ee 304, 324, 406, 420, 421 
copper hydroxide, see Kocide 101 WP™ 
Cott Belt ..5 ies 5 Sis A an ee Sorin ca lon bans 1c PRON OS wycheye come captecaeg ene ce Colieh ah tpg ge eh Wy 
COTY OM oso ancte Sure ites duro gous guveilas eHbve-4 dnb lo ate be ca my oc hvemnpon sey ey lle re cope ste RSA ge ae a 525 
cost 

of Bacillus thuringiensis (Bt) acca tisen pee nie Seer edhe wee. 0 enon tee eee 430 

of Douglas-fir tussock*mothiNP VOM s ..tsoctetvars- cecte cer even sy sose cms eeah vas le ene aoe es ee 436, 437 
cost:benefit analysis/ratio (see also benefit:cost ratio) ................. 27, 29539; 39, 42,44, 120 121 125 
cottonseed Cake hl. oa sye,s penton aaa aad tenuane cagepe) cacdiggs forak Re kone aR ey Roe Reply ee tone 93 
coverage 

Li = | eaten pele pened Role I re eaby oe ARTE ier sno ee Aes NS Fae eal wo te 276, 429, 430 
creosote treatment. Of WOOd © 228: Capote co eres ite ele ce esa eon hae geo eee ca ee gee 464 
STOSSAINTO CEL VIEW! Tocsiccreeceste Gy sl hos, au. se ices: « ston oa tes eh tae) elena cane, echt D ga BSP geet oe er 415 
CTOSS PFOLECUION od adiscta y's GN Aye Gash. Sik Mises age och ogee NE, eee ake (Oc Wea I edt ne pe ne 14 
cross-resistance, see resistance 
crystals (see also. Bt) cisshidic ciccass boo -2 Acedia there ister mieten atten sacks eee ene alee aie a ae a 429 

birefringent (as diagnostic: characteristic of. virus infection) @-. ne )osesen cee aticeee es eee 283 
cultural control 

OL MSECE PESTS sof Fog. cancseenedle laa nesehe ade eee cea RCs ¢ PPM ct: Sense 2 RU cl myiteny Mace a 25 

OF plant Patho mens: 2 icf hak as oe aves vats se cee aie tenes rete ote Me icy rat eens Oc ements 40 
D 
GAM Y 5 2G sien 56s FIs Set dear ve Ge ad god PR eee RRR: a oO ne CTE, ea SR 64 
damping off, See‘Taxonomic Index also 7... ur mene See ee enacts ont ree ee 94, 96, 117 
database(s) 

OM BIthrOpOds Mss sess y7 rest tees eae koa aba Renda wep ie etter cs oO annem Reale okt ae en eee 155 

on. berieficial orgamisimsite. 40 Ef oS ice aa ence grey eae ore eleietaute ee vce ke ee arg a ote 155 

on ectomycorrhizal Tung 269208 1 ChAe crete serrate usta caus bee tag cctaeey tates meee eke 460 

on entomopathogenic fungal cultures ccs oes ese ee ee eels va eee ee iets) 

On. Puntos SN eT ae 5 ik os See eS Guage aceon aN, tea Siu omeue cu ae arnt one cg ics et ee julie) 

On immigrantnonimdigenous arthrOpods..7.5 eran. mene nist ele oi wate peeuse nee eee 1535156 

onrneimatodes s 5:6 Sieh Lec yee e kook iecee eeie eoceee fe ete ete ee ESS 
DDT (dichloraadipheny! trichloroethane) i, -4-1. ec ee ee eee 18, 102, 417, 424, 436, 443 
D- De tx tree si bce bce encase hasioteoiiagd aS DD GIOT Oe Ano Mek Ute ee Eee eT a 22 
dead wood (role in supporting predator populations in forests) ........... 00.0... cece cece eee eaeees 449 
defoliation Mime Sat Beene i ee 106, 113, 418, 419, 425, 427-431, 433, 438, 439, 441, 444, 450 
deéfohators Sieg Steere te teh Oe Sere eh eee are 102, 110, 112, 113, 116, 414-416, 420, 428, 430-453 

COMMER PNR 55 Getik tat isesnn Adak Reb eie ners Psa gee ae ie ee ee 113, 116, 428, 432-453 

hardwood t Bact arwe ren 5 2524 26 5) eigen tena eee eee ee 110, 112, 414-416, 426, 428 
density’depemienice’s ve Lote. oak hese cebem peut ttn eee ee ee ee 1, 398, 399, 403, 423, 452 

Spatial Sul s'595 SER Re ke fee SE ENN ae Nha ere cr gt eee nee ele eee ee er 423 
deoxyribonucleic acid, see DNA 
detoxificationie tT R ees oan tik Neck een evealetiadtea teens cdeeiited oa untested eek ae cee na a 458 
Gevelopitig COUNTIES s.r, ove state's ei9-0kg eae ecepecceseeee eae een tone tose ae ree eee 460 
development time/deyelopmental rate... 20). ae eet ee eee 404, 429 


564 


ORSORUNS 4c 1 bogs SS Gh fe ek ean Ce em Se 417, 443, 445, 446, 452 
dichloro dipheny] trichloroethane, see DDT 


OT ete I GR SE a eee aL bees % Ahk cue ee oe Maa AL 106, 425 
ae Meee Meret ice 92 reseed hers Nie OA na Eo REAM wen eh 320, 451 
diseases, see pathogens 
iminpec tamtisINteClion, awe ware he ORE le Benen Rho vie wae we SANS Vad dae 267, 278, 306 
LO Ie See A ee ne 9) Ronee cece eee ee ee eo 127, 130, 431, 441, 453 
SOO Oe eRe Ni ee eee he meee rte nes hi leks Beha dude h aaa Ria alps dee Ma haw Cate Sree 431, 462 
SPST ESTOS 1 OE ONS Gtk bo Bye a OS I es ASG i nea ee ee ee a rn gee 460-462 
Se ee co a ae ee a a ee 401, 412, 420-423, 447-450, 456, 458, 460, 462 
DNA (deoxyribonucleic acid) 
ELC SEG ge ee Nene i er See NM Shee 2 Wk We en eh When oa, Ae Oe ARLES 3 
SR LACMPOMIOSOMA lL Vat spe Ny ee RE OOS elas Te One Ch SEB LS ale ak devel oad Wee 300 
PISCE ONSEN gt ee eR eee Ree Ee hn at ney, ation a Sea Glew adits S05 aS eee Hoey ee Bh 
LEIS ED tet sy Ae Gey ans Cc gr akan 0 Tone cro 1 (7 9 Sa POR enna na 300 
BLOGs Vira meme omer Een ne i ee AL ES i sien aim windians sige be sven SEE aS S13 
recombinant, see recombinant DNA 
OSes SDOUSEICHEY CSE rrr eae are Cer M A BPW AEE PENA uc iemra rans dah w deldaie kbs sons e & ese erence 278 
BEQELEEN oy go) oa RAMEE Air SAU PSR ce UO Re oh Aer ORE Ce nes cr Ad 106, 458 
COTE gs Sop ea ew Ate 7 RPA Pare e arc Se a See fr 54, 58, 64 
ey EE ee cae, rice eke eats Cr tacusntes ok ets a Sd ioe Bie a GSse FANG PO ey AO He Se alm oies SON 304 
E 
RCV SBOE se Pte can Foy earl at gu vi pda an apostate asad. Buea. OR Ee oe OL eee 426 
COURT CIDeNC Li Smet PRR ee ww, 1 ENYCE. cally: s1F8- Tubagonte oa aet ssa eabmhas Wes as Noah PS Sey a 264 
Patent ame ML AL IO QTSALY SES Mtaye aca eee eas Ses a <; SG eri ER oes veda ecko Ade, os 1232128 
AaGHRErE CRITI UTA V LEG re Mam iew er bx. cd yk feo x tbe cos ir Se fo Sh GOIed maa de ef earre de brs Us ein eg RE ES 128 
PO seein wiene caipLOUUOe ) man miee teas re wee Palen Cte. heim nee toed i GleRlls Git leledin OS Mosca cable Bee 22. 125 
efficacy 
ES CaP Beha cra Pe pods eo tate ke Gate Moke tn HOO oe wl nto Mee 115, 414, 428, 430, 450, 451 
COMIC UTT SS SR ue ef gE ae EAR Wot be alls seem ante Sue Pees bdr OR tana lave Ales 424, 426, 427, 436 
Fe Gic FnaPP MRE NR ARAB 8). soc el pv vente, « 05- nle S  oe e oee ay eb eee 288, 319 
Ree CIV GterOiCre WICOSVUtranliet ase) Dwain face onll cwiay aide sv aula aku he etekins tree one eee 426 
Bin Ui vOlO Rare wen te Clee ie eR ee beet tok eae ih Dh Ys bine al aletbvlae b4 ca boat ok beak leew 396 
PIBchCemeyeamniOvizatlonsOl PesuiClde UISCE Mame a etd rte unie Abies Saye ecw boa Reese’ ck es ase ea pee 8 436 
encapsulation(s) 
CMC RCCI AMOS mtr Pott ne 2 eee, aie nee Lacey sisi n seinen lin WEA aerd Se mE Pace eye @ & a GWoed NO 32 
Seas Cas INU LOI MEME art nde elk cee etek ih hia sige g see Sle on ee Says 276 
OL bidlogical control agents (as.a production technology) © <c.cs.6 2 wee ee ste a ee ele ale oe 91,94 
Pee COLIIS (ALC ME) Pert ie Et cone kee Lar GN ede ice Wo idts a0 'RWE ee Wl a Sle > wlan 289, 290 
Gr erVirie taltaWhiearen CCT nae oie ewes Meet aA kn kat weyers irate dale Tle gets Sotata fd Sky's ats Sos aisle ecaauasoe Be ene ee 1 
BG Hg PAVE LIS@SuITIISUIISCIGONS 0208, EE Pian eet. COR Oi eee Slew ok hee eka aus 5 Ms Pls O26s19 
Beara sibe lose NOStSEEE a rua eae hme emnn ee Ty Me Gee Ries anit Shite wee vio eMlle setae © eh eee 30, 444 
Pe AUC SECIS DOCIOSHACE OL AO) Data dt cee eee ne Gk caitlin Gul ’s she Oh Shes ee eaten Jidee) 
Seige DOU AIONS Mine pee ieee: Wel hale. Aico Na ote pts shasnib sv lelade ian hd RDG Mes Veet 398-401, 406, 408, 439 
ae oe. oo culag cy APR Oe ee a oe re Nea 92 
endotoxins, see Bt 
SORE YATy Cec ae Cle ren See CP he fois Lotto ls iase whens le wats Wa Vigra s tA le dats eee ew ee ees 427 
Ma NAREO CE Ca ALUTaL CNCOMES cetrcusny hike = i Gbh wy nak baw bjaswebindslin Wh Seu ows sents % 106, 107, 397, 446 
entomopathogens, see also pathogens, insect ................. 106, 159, 287, 290, 314, 317, 318, 329, 423 
LI ll IS fei fo 8- 15 5 Gases od 'a rblle dba NIA Weg seein tal dbo toa do alate atvih fe wlesuya tah a/s 288, 314, 315 
Be OAC eG RRR ect PU ee (Joe. fatale ais be sits atin ye Wh Wiehe ela eke Sold n Sle a les hagas alee Le Bakes 397 
Prvironinent/ environmental c.uic se one ea ae awn tle ca eee os 127, 132-136, 146, 154, 159, 407, 409, 411, 417, 
425, 428, 432, 436, 450, 453, 458, 463, 464, 466 
SMEISSIKS soo aA OLS GU POOR UK EE O MEE DORR Cn OOPES 2h Cos Ran cia one ae ee Gee 135 
Pere Fit Sa re I ewe a0 042 Ree. Fs Ss PP Shese, Nis isa oda Vo ae Raed We dla hw alelale BM lower es 264 
Beate ami AttOM POL lUtION Memmi, hia Pee re tal» fikre scotntincs tidus oie) slowly min cov lahe es 47, 49, 103, 108 


565 


damage from. classical biological control’ gi s¢c00 sc. 5) es 1 oe soe See ieee ene 154 


STOUPS oss cs sae ea wade CR hee OMe Uo wma eae also ee ee doe ene 6 tee ate nne aie ene 134, 135 
manipulation, as a control technique = «2, Acc0- ses 2 se) es ny uae ee 31, 41, 65 
studies for introduction of biological control agents .. >... .5.. ase. 2-040 tes spe i 154 
environmentally-Sensitive areas. <o.cis.6 ain seas eis = aot obey ov 28 alee dos 0. oe les Ohms (one or ena el a 430 
ENZYMES ENT o-c5 aso ee Reh So Sas Ee REG PGR oat pee 273, 274, 277, 310, 311, 313, 462, 463 
OXO~ sarde Ate Ee SRR ise aig dx ie avics uy ouenee asee ees Wel ah so hate ln Fasenas oilee be at ee te eee oe ee 464 
in disease, development’ {3 .. 340. ¢,1'5.0 gr are «Soe, eee ooo aunts aoe eee oe Sees Sr 4] 
inhibition Of 45:53 oc dose auseotlesaloing aed cope hobs ae Cathe ies Rose ute tee eee ner 463 
PLOtcolytiowh wenk-Fe a. AOk CCRT 1S, Mee seals ao oe bo aie Senne nee aire ee 3119328 
enzyme-linked immunosorbent assay (ELISA). 2.70 W oa 2 gt aes se ee ee ee 293, 434 
enidemic(s), seealsO Outbreak (S jimi. hte eee ee 106, 395, 396, 398-401, 404, 407, 408, 443, 446 
epizootic(s)/epizootiology ............ 281, 283, 286, 288, 308, 309, 312, 314, 315, 325, 327, 419, 435, 452 
GTACICOTION S| ie ogo etiam RN he ti Cea cee ata Ns Se ee ree 125, 135, 294, 416, 417, 424, 465 
establishment 
of mycorrhizal fUNGi 4. omens wo creas cone bee F Seema oe Stee pees Sr 460 
OL natural enemies aa. qemay ee 52, 53, 56, 60, 71, 83-88, 90, 120, 122-125, 127,130; 145; 146,260; 


285, 294, 314, 396, 401, 410, 411, 416, 418-423, 440-444, 453, 454, 460, 467 
ethylene dibromide, see EDB 


ethylen@ Oxide a: 5. ernie i ae ae tects n a ear dah ek trie 297,298 
evolution 
behavioral |< :.(o3" 455.002 Rees nee ee eta Oe et Peels SPS «acai ate nes ae ea 418 


co-, see co-evolution 
EUP, see experimental use permit 


EVeIi-ape SCANS 25 fevvct iyo lgote ake vdane Pol aie rani Surin A eke RO ousleleeadeee eed ERE eke weee ee 447 
exclusion 
CASO So wen ree tant tte As tes Seti) ould Or Lear Mey. ear en en ae en 129, 403, 449 
MSO CICIGAL  a.ass, os ahs s. ke ce NS Gg wie Agl Gee wits y aaa san Bus ae Pues la her utes Pedteas sc te eee e 129 
emnterference teChnique yaa c.cts oak Send an eee a aay rahe nee he salir, ee Ane 403 
Executive. Order oniinvasive SpeCieSas 42 Wnt ese umeanany boa ous a eee 154, 155 
EXO-DECVICOMNM Ri 58 uence aig ed ws tell ee tg aed lien he ok IR cea see ee a PO cae 400 


exotic natural enemies, see natural enemies, exotic 
exotic pests, see pests, exotic 


Experimental Use Permit (EUP) raat cnet nies ese ee oe eet 310, 327, 435 
extender patties . 21.21 Gi acesga: oe esd uw sig cs os uuange cia co oer Sueur ae? Selena eee nae 274, 329 
F 
FAI Y TING oso fea teak, oo oleae eats de dint rope bas Seno nate ge eUvcaytens cals [fe acelin ce ped to 90 
fat DOdY. betes ese aes ai ninieie aca 8 ue Wis gla A Sep aahaleke Gnaylitceet psi <p ane cele ale Ayia Sg er mee re 303 
Fattyc Bends. en ee cge Seis aie litre eee (ae eae aac Rann ee 274, 293, 301, 403 
WUNS ACU Ate as cs, 6.5.0 ie v0 alge Bhs, Ge igsidie, © Guede Sys Sita sah foseuas Sb ene ae Lo 93 
POCUNGItY yee Oi: Foca ha ok Wale tea Nh eee CES kt ial Sak ee eee 277, 291, 312, 319, 405, 408, 452 
Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA) .................0.0000, sates Ts RA 2, 46, 67 
Federal Noxious, Weed Act ss 34:5. sua) ven ote tlsae as stteaie ts tas Ae cea a en 128 
Federal Plant Quarantine Acts icant cue «nic ede Lew dee saa deer snare ene ade ake 7 
Federal Register iii :5 <acs Wend oasis atvie mint itis yale Cea eis daptks co ete). SNS tee ae ge 135 
feeding stimulant 5 2e.cas).n.2 cings 4c) oraeeelch hey ES Aah, age scl onels ie ae ty er 290 
feral:colonies of bees 42.0... 2... ccna eens cea ote heae @ Ree 21552769325 
fermentation | wast. « 55.5 5x5 teats tis Wek aman See ee a I 274, 289, 290, 320, 321, 323 
Liquid g.35 ues tars int. daha: BC ARR get y o) ce 5 32 a oe ae ele cI eine ee a Oe ae 90, 94, 289 
Gert litys wcakme ss 5 ip sie am Sek oe a see alee eaten age Sloe gc em Ge tr RN ee 405 
fetal bovine serum (FBS) mies sated hate israel ee 301931] 
few, polyhedra mutant (FP) At sam. ng Ata eet. ots kl ee.) ead ol ee oe a ee 426 
field Cage a4. wtzii0 Mean gt hekei AE Be Pei ot ice cleric ane Bc sa gghe te aoe mms ah Re eee 129, 443 
ERCN COWS is civrissitstatin ncn, x tga sca ees eet ar ea tee Nc ate eal ere nee 94,125, 413 
Pelt TCS oo cs osc facs sass teun one Ge eel a aeetem tra es enero 0, Cae eg ea oe 329, 330 
fire (see also DUIMING) ia scare nisi ceoccde code ants ee oie ee A a ce 107 


566 


eee a ne ee Ne ee ae es a reas Fo Fie gute eo  Agraaw bE owe dere vale open oe wa DAO Os 400 
CU IGE SSSI Aa ge cae, alt ct eer ecg eee eo a Poe er a ce 288 
ROUMLG OT CILeAtnentl OF PID WOOd emetiatit: sitelaeene can See elas, fue ES gia mee) MAN eis 28 463 
OEIC LT CALC ALCL OM ore Sle eet EMR IME os aa ko ahackle wk dete abe GHA Sela whoo 274 
TUNES SITTERS opine ech loeeil (lag ocr pk rr ga a 130 
es ea NM eI Ce et Fs lee yen ye cee eh oe po 8¥ 54 4 yh a Aw B+ Sv! vier deaaeve wane ane BRAD 307 
rset i cy eer E eee Vig ey ey ore Me IG Pees, Seale Gls eis Ok Ge chaste Hed ES La ae awe + 458 
OME LADO OCT ON YS RE Mery e nree ernie este iemNe ed MEY Sic. xtviglih oh <)etei x) oom ska asa Stale erie eee acs 27, 466 
Sere eI EE CIT ALOU MMM Sere Ld itr te PUREE. tee ah creel Ue BV Rew Del's MAD: wile Chee Ai EE RE 448 
foreign exploration/collection ......... W5=19525526,28557, 445,45552)54-575:59,60, 67; :70,°72).73;- 76470, 
80, 89, 103, 120, 121, 123-125, 132, 146, 150, 152, 153, 331, 417, 466 

SOL OSIES me cannes Gsm helen a ese denny ie 8 270, 315, 399, 400, 402, 403, 406, 409-412, 416, 419, 421-424, 426, 
428, 431, 432, 434-439, 444, 445, 447-450, 456, 458, 460-463, 466, 467 

SCE I Ca OEE, uLE nie eS NEM a ara RARE ria a hey Se 5 Mal dbs, ocGd ap arash ae vgh Siaiespnpndin @:-A8/ oles peruse wl MG 422 
Forest and Rangeland Renewable Resources Planning Act of 1974 ...... 0.0... cc cece cece es 435 
ROT eR LSM ICOVCINGIMruitgme Bi TOM bes chem AMI rte ch atti st st au os uglesare dev! 400) ac apacas aaa MOND BRNO ok 466 
Forestry Research, State Plans, and Assistance Act of 1962 (McIntire-Stennis) ..................005. 101 
POTD ANSON CORE Reet an SPP an En IE: rian Age Gea Hl es eh, Leck SAMMI G ceva os, vin a Ada ale Dawes.» 2819319 
RCVETIN ALI} eR RUDY xe ei crn dena a td choir tS A Ube yc e Ania ket MEE co keira PTE Ge aul 281, 448 
POR MIUUACIOUS ete re oral neta peel WR cgcleyep ico see coe + 159, 272, 274, 284, 285, 290, 291, 299, 301, 305, 308-310 
SES Cate cette ah RO Es or dSrae oh a8, has ae dh shes sh Sptjacsive 34, 35, 290, 291, 292, 427-431, 450, 451 
RS I es etn ete aig, aR Nr aes yew, 40.%, @ ae, SoMa dln his gdp wt FRSOre Wicboe ees. 284, 285, 295 

DCH NCA Sim ne eM ear e te er E nce udetki ae Kae kein Hida S10 & bc von ale EARS 406 

RAV ARUSES witiee > tibet a5 psi atc wee ae MM A A OT ate 277, 280, 289, 319, 425, 426, 435 
ori es it Pn Me, te eR le cc ge AT ee sls eo sey ests sp CRS WG, 6S Aseimn w/a IR Dee 400 
rt IEP PM ig Te a AY Aie nye ot a's (a inven lh aia ae wR Kemah oe whe 66, 98-100, 267, 466 
Rc Ee De es ie cae aie, 9. 1) Gpalie Nyraytuk wai BAUS! cise lO aes gles 159, 279, 280 

RE Sem OSUITULCLIGE)) maha catenins Sein cat uruis @ bent Gyre a2 ore Noe aya 398, 406, 407, 414, 456, 458-466 
CNETIEDOS UOTE The nn cod ama oA ney ES SOR SOC TCO REE ents OF et eee ae Se Arn) CR Mae a nn + re eR a 456, 465 
CHIC CHCONLCCIOTS meeenem etree ey repeater ey We wiss ce roles sis, skelter Wi RYE EW an eA Rites. Ala wate apaes 459, 461, 464 

PRE DINECOTTIZAMGEIVLL meant yee teeth fie Keisaiishe a. Gusts Soho he mares ele ate Rem ack 117, 118, 414, 459-462 
ATT AU ASC Me mee Er Sn i a Lio ch Ocha cl pingn ere gh esas Sie said a ohne as,» Oe aU 287 
STOOUII 110 MRI ee eek oie ras ear ea eis io uate told a kes Qk emi ess Gad We 71, 72, 96- 98, 119, 291, 457 
SALON OP ALO CIC mek eee rR GaSe 5 Ge inle-e (Ow outst eaiia wn aw 54 ain ee 5 70272359555 159, 414 
EM GLC era gear AR IAI oy ho. Fils psa “tpch oy Sods = lest me Iecee le 1 mn W aes foams « BOND 96-98 

Bin eer Dal aSitt CMe ree re aa eet yy orae cine waar iol w WA Sin N Th ale a sag «ih a, hal almerew auwle Ha b's abel Ble Gl 456 

Dy POgeOUs bolOLeHaneall) Wry ee Ne tA RN hated Aasd 1 On Eer tothe 424.865 owe bh, 6 Ewan ere Melty oh 461 
eLOCHOUS COs STASSUODDEIS ae hey eh ee an eM te Relig be fone elo ti rsis OTS. nts Rion Gumtree 159 

TARO EOSEA LSC OMEECIIAW ILLMME PenMra DARI TUT cca tay ccs et CUEP A scene ies alte te nine wo lw wy ess a ron 5, ROR 71 
Dae Lie es oe ats AISNE de ofeach spicy snes al AYN D Shey Tee a ew arsg oO AT ole one as 96 
CAME 72 eee ey ei cic potoas aetna Ree wom aie 22 ala hyde o's ieee AG oe 105, 117, 118, 458-462 
SSTTVCR TAC OLICN See arate re Aes a ie ape eM Valea tts Micke ena tioalwittieferw is wiajeeronel eos, 21, 92 
DS ON et a Pras Pr res Reels ito a os pede Gigs he an dpe et rdo de ins nase ts enebe@ eels 9 ROME 457, 461 

Fe I pin a pe yeite IRAE up roe Phe deo bduis «weg erate 93, 95, 98, 99, 102, 104, 118, 463-465 
ean ea eM ALY CLIN Mare age oat Week casei iors rah we oe A ew Hama oe oA ale i Sie Me ne 465 

ey No eR iat yep SRL, = Iv vecn yee ams Pes ae e > + Die ale didiegn AR, sadn ye, oa ee 458 
vesicular-arbuscular mycorrhizal ...............-.5: SPRL Brakes: haan eaincyayedige An ere 460 
DUTRN AAC MATT OMe eBay hon fe cwoifins ss IS As «2 Sod Sat MNEs NE ein BHO odebon ee SR 463 
NHN ADO AY EN MMP eet eas 1 saeide Jos tn sd ays cesabodn wns fei evecn ile fo Rye lode 105, 107, 118, 463-465 

Eee Ved wi ITVAN CUT) OMT eee ae ret jc pe must Fave pea tate Ar acti Sona sh do les ps 98 pnts hoy pn edebe LAO 456, 463 
Sra SL ATTIRE eee Lee ey Labs Wane eae ode eds ee = BS fuiee eee EM x ome 106, 119, 463 
BRE OCG) ee PAS AE os hee ain os bene Amira ahr ips Se a VO 71, 93, 94, 96-100, 308, 326, 327 
Bras Til PE eile thse) ates 4 2AG6 Sel go alae 4, Sam 09 DHRU SNE aN cr MIEN LOW hee ST 98 
SeeeeaTer a ID IRIS Mere terry tare tisk 1s, An at als doth of ue wight aes Ait (cles (sin isleraiayy | AMUN Mah a Oe 96 
urareeaiera DOU OT OIC Pewee BuinGms Cle er apse: slag ichea odie eta arue-e Rad tae At 465 


567 


G 

pametOgenesis 6 hud ffs aated Ce ees SoS ee ev Eels ee ceed dae nee ae ate eae 295 

gas sterilization of bees wax combs ....... Pree Pere er 328 

genetic engineering (see also biotechnology, protein engineering, recombinant DNA, transgenic) .. 68, 69, 71, 
90, 94-96, 149, 299-301, 311, 414, 425-427, 451, 457, 458 


GlioGard™ 22.205 veda vealed eax edad aglalpnee leas kas (dae Lee ne 94 
PIUCONASES «cis fs gia cE Ss SEs Hea Hee Eee Orta ae dhe wale eet a 6a ate amar ee 457 
BIICOSE Ve eT eA a hie ck Fics om deg Pla Ee On 8 AEG eal es OIC ee ene are ne ae 464 
glucuronidase (GUS), beta , ., fs 6ccs Wolea ta cig vibes ooops ees aed Page ees 4) oe 414 
glycoprotein spikes «2 fia 22 242 dc Lins Bie olden el oe ee oak ae als 9 Ce en ee 301, 302 
Brains OV. cies dace oe coh Mate Rae Tee a eM ns oe Roth es Sine cae 54, 58, 59, 63, 69, 70, 84, 288 
small Gott Pee Pees ORE pe tee Ae eae WS aoe pene aan carr eee eee 121,124; 129.307 
stored P8270 PoP OR LES AR a i ee ore eee 70, 159, 292327 
grass(es), see forage, grasslands, lawn, and turf 
Prasslands ee ho eens! < oh v.58 eo Meee epee, o, stead Re ee ee aha 21, PO ee eee er 102 
preen' logs 220000. Pye sea cae ad 5 5 ee SS Eee eee 465 
ground water contamination... 64. cceeee. $Oe ds bed we see nee es 62 ees On re 67 
guilds/guild formation ., ... s+ + «»feieBeelae ots laeteuNe 2 tame ts. Wee Sm SU gs err ae One ee 422, 461 
EY DCHCK Ae ery Nae 0 te eae cece em ere seas, Feel nan 103, 106, 107, 111, 112, 424-426, 431 
Gypsy: Moth Life System Model (GMLSM) 5.235 wins 425 oes va ee ee eee ee ee 422 
H 
Halogen’ etc sce ee ei wis, ord dontnry. ares I aja ost e SiesS ote Sm gee oa ore ohne ene ee 326 
handling time 105s Sees eae eee odie Rate wee eb aye eet Dep aoe. a ne ace a me te ee 62 
"Healthy Forests for/America's Future" Strategic Plan (Forest Service) 2.5. 752..-- +7 .4-790) eee 106 
HEP Athtrationio a0 202 tiie ae oa ous ee Exam te toeun: Scie ic eee ere eee nag ae 424 
hierbicide(s) § its Mais sie e ac Eko oe lark ees ciate ee oreo te pe aye nan 87-91, 123 
DIG BE Saks eo the Revie ts £28 e0 a0 te See Mares Cebus Fhe Oe Rae ee ee 87, 88 
NY CO Fo rn tes are tes Be tS Rhine aw aighe a ae BoD earch debe se aai ees One ee 88-91, 164 
heteromorphic forms F595 2% oe ee Oe who OC aibep Spam esha GAS Hanus oa ene yas eat eae ee 407 
hOMEOWNETS? ois 3 ee Su OP Ene ba 2d oe ahs See Sk eae ee Se ets ee eee 428 
TONEY erg es atts Rae S ete cee eee cae eae ete a co eee ale «ttl tac eres cen 274, 296, 328 
FROTINOME(S hs eae, eee coho he sai @ Seite shee Yoke wen Eocette Batak SAAT gests Tee Sacto era 29, 462 
developmenttalin Cees fc ute 36.0 eae Be eis Ba Be ei ae eee eee tees ieee 303 
insect MOMINGN. {sh ccdd. Gas od, 5G de nome Re bcudhe et oes 49 te dutsdeun is Bree ekg ee ne 304 
TOUT 7 ass: 5 i patois ve shih, 0 bigh aw th a Settee Seer Laie Neue ttc ae an ta a eae cee ene a ra ag 300 
host 
alternate/alternative .......... 104, 106, 111, 112, 270, 271, 284, 295, 302, 403, 410, 420, 421, 445, 452 
feeding 2a aesawsd Ree fae REPRE A Ba elses URE Bowie ae + ae eg eg ee 271 
TANS oe Ae ees eet ek ee 270, 277, 278, 280, 282, 290, 292, 302, 303, 307, 308, 310, 312, 416, 461 
microsporidan *. sie) eg taea ties ee tae eee Pook eee AO eee ee 201; 342 
nematode tits: Coos od Shad beaks BANA Ss tea eo wil ee oie Sne e ee e 278 
Vitaly yak b Kitaeh tat tate © Sete are Bie te ee Ne cy cn en 270, 280, 282, 303, 308, 311 
SECONGALY «io de so Ln dics jis Su RRS Ee abit cera lene gts eae os ene ee 453 
SPOCHTICIEVAM,, = Fe ee ONL ie tote Cee Od ARERR Rae RO Ree CORE ee Oe 276, 286, 308, 437, 461 
susceptibiltycs72Ata.s se CRA IRe et ea Ae Ook 2 te ephne hee ee sere eae 304, 307, 429, 430 
host/prey 
GONSICY S2 esac een RAGE Beis BG Spe re oe ewe ene aces eke 420, 422, 445, 449 
preference: s..32 Fis Badd sae deed OR ee Picea ae ee Ree ee ee eee 403, 411, 416, 423, 455 
seléction YOS Ol ina) ni reo eee eich ae ee ee 32, 33, 61, 65, 66, 103, 422, 434 
hybridizations staso.5. 204 0s5, cdi usd Sees ohideae oe nee Ce eee ee 289, 291, 295 
hybridomas 7.25 oe tists ane,sivbid Bae Siw wig wes dn dete eGR eRe Wade G Male aoe eee oe ee 323 
2O-hydroxyecdySomer eH. F 7h 6 Sesus aus iat bbw vesege Abe ss Mitade WR cade sth teen ee 304 
hygromycin, see resistance, hygromycin 
hyperparasite(s) 
BTUSOCE 5. veic onus souaiel 40% soheptuti ASR, Saean ieee IN ecto gt haces PR Eun 419, 439 
microbial}. 2. as ise tie eds SERS we doe be tales oa ee ae 456 
568 


STE RPOr SU) LUT mE ot aR Ae toe yA tex vcahah ct ah Geni 0 id: ale iao eas poiev rn erae at dh! ap es epee w ENE ale aed 326 


SuSE ELS SE as as SBR RU Bn Oe ee 105, 117, 456 
I 
AURERE ELPA LCE IN 1 SATS OST A Ads ee ES fae os FAT GE ar ae H! sd ats wa OLE ele ue eared heen 273 
UTC LUSIOL Sen Se eet NO TR Re Wide dials coe vena s LAGU eR en ae eR E we eh 403 
SPORE CL OD LOLES See arena te ORME MOP aid GNP aRe Oa vets wie deve ges die wae MEA ole Re eee 403 
impact 
rad COMO cr ener eae Rr eC OPE iiss Gis, iia e aa dae wk vee GAN 132, LA7M1S4 2155 
CVT AUT CMON TOS yee 7-0 25.10 ,) seer seh aahoiamsbloconnl op AGH o'er 30 129, 130, 395-400, 402-404, 407, 408, 410-415, 419, 


422, 430, 431, 433, 434, 439, 444, 445, 447, 448, 450-452 

importation of biological control agents, see also regulation ... 24-31, 33, 46, 49-51, 53, 54, 58-60, 67, 73-76, 
OleLO3-10S 21075110, 120, 121, 1 24R 13251458154. 

156, 267, 268, 289, 308, 395, 401, 408, 410, 416, 417, 420-422 


PAvue eid OlGsaretyeCOmnimtee (IG) DTOPOSed (ainda ee acesiae neti ed tis win bale e by ce clelle 4 bom Cam ee 322 
in vitro production/in vitro rearing 
Pent ets SPIT MIT OLEVISIGL SLA BEA TER A he HO NO ress hi MDS Aw Ae Bua aw’ ven ad BOM Moe 300 
SACL Chi ame EEE cea new Mra eke Pari Pid peed ka Owe onde wwe es ova OE 92, 96, 98, 290, 315 
CUEING BS Be Se SE een A eee ee eee rea or 326 
Sais ca ea cae SPAR PED Ae eck tee eects SMM eR Ke a ep aa ule a bee ees 65 
PO OROSES) 0 So 5 WA 6 “Se Oa rete cesar ng a 695 727271,302,.30383 100311 
ects pO OUILe Sen AMER ieee eo AeA aioe ee wwe sade go nda wela wie ew ae 280, 292, 293, 319, 435-437 
(TEST INEE SSE TETED. ots 2 ee oR cae no a Ne ee ear ee 129 
infectivity 
EAT R RISEN ICAL) Fe Rested eg Rees pot yy Sn cuore ert haa se hen © vou ee Ye eM EE Sa Oa oe as 284, 415 
er AN SD ey RN aa FeV iene en a1 ot sane sind iG” doe PET Gea ds ed WE Sy To 279, 316 
Re ek At PY WN toes ies RTA he TH: Masts sw CaN OWE OO bb aka, p's WINER 31593 168s1s 
OR At Ee eee? AeRath nev eas N VTC Rarar sein RAM RTS ie ces vie ase RU Ri eae aes eRe bad A MRR 311 
CTS ENG CLE AMON grape Maa REY cdc na Sah Sc Wha sch aI ee veh dod oH NE ac ah WEIR tera Monend WEN, Sime, 271,282 
ah SER 3 RE MRD ACERS 21 ee ae a er a DIAL 219, 280,282, 302931 137318 
inhibition 
BoE SY EN CL AS CMON areal tl ta RAI Aci cet: end oa oredr oe Phen late Tor dk yige a GI eee, a 463 
Bo Grd I RE eis hci i oto) ysl ts eenceyhecPooans Wake Avo) HVE Sa ¥ a Glee bow w seen ee 411, 452, 465 
PRINT RM ROY TILICSIs ebante uli oda th ascantt Y/sioad ten): sft esl! Win) goa ais 4 wack 5: AOE Shes oo bec ce aS 302 
inoculation (see also, releases, inoculative) 
BeOS ORI AlSMissiOM OF INSECEL PathORENS sx ciis. wakes bein eee Fees oN asin 281, 289, 326 
Sen ERMAN UNTO Win ota ode hee Bebe etre erties idee ates GALES eA A on idan wea weds 117, 118, 458-461 
SAUTER VATS on BUS en cee ge en ee ee eee ee ae er ee a 281 
ee nT 3 Oe fat eee Pn PO AS ne PS vie ate Pb Ha aw ole! og PONE OR SRI AE 323 
RU El Cae EER ol re -8 Ac ana fopaleitla Sida nteaueia pm eoh ey wea Nas Buh eS OL FOV R Me Oe heehee 427 
eee LOST ECORI S| OBIE Ga ce i Ne op Lois legh wins SAG: fo atv wee oe Fis wisp de oles 425 
imsecticide(s\/inseécticidal ............6.00.. 18, 19, 27, 28, 31, 42, 44, 58-62, 69, 70, 102-104, 106, 107, 113, 
122, 146, 272, 308, 312, 320, 321, 402, 406, 414, 428, 431, 436, 447, 450, 455 
Skt Ne SG eal fv rssh ehenactins Beraye Vas et aS We Ge ae eae ee eek ON SIZ 72 {415 
Re 1d MPR PI OY Serpe e tcary bo HA Gin Deere Ps Paces kr Fee aed Hyd va wo See 292, 308 
SSC rl! . REIS Wee ari aera ee ana ee 159, 272, 278, 282, 308, 309, 316, 319, 438, 451, 453 
ERECT Sciacca een ee eee eS ae ROR HE URE oRLG erly Sd WT Sod ee 429 
coon og cob iat SSRs, coca Cae Sn ac Oa eo a ee 32 
ECT O Die MPPMP aetnc naa icay selahbiar iersiave eens eG See 70, 107, 272, 285, 309, 312, 313, 424, 428, 431 
Sede ee Se Ly ce. ea whence wee din ARG ND ea eMC ae GH WE a Cam Rew 10 side a Mos 69 
ee RE Pe Set Riel Sunken eg oi siay HAS LES x Teme w dD Toe be BREE h Vag neers 310 
Pe eT nit REE eee ene ide ae aOR US eked v-dx Saistrenle sees ais Randa peo eh 2 
ee ret sl eet Nae ep tla drench ystsna phe ore A ierd 9.8 aS aH A 104, 106, 113, 308, 435 
insect(s) 
aera Re eg OS ae AP aioe hace le Gg CSN io ls, 014) o's bie oes Me en Pee eee 266-268 
OIICDNAL OUST TY, Siu bam Mes RA How HERERO ERS oe ee DERG Shae Oe He 3352561205566 


pathology, see pathology 


569 


MANAVEMENE 06 sos dee sce se sre deeper encysy a on es yt te yal abaya e gaiek at op thag a) 7h ace Bc Ales eos obatea ry Seren eee 261 


GRE Arid COME? re kee cecicedoh Seg tues, A yo -eulsndvaglle wok. Spee ccltenalowe- 2, 3) oie cre area, a areing ear alee LOL 102 
systematics, see taxonomy/systematics, insect 
iS pPECtionye hss ees. IO Be AEE Ld FI Oe tai line Ee reciever ate de ee ee en 268 
institutional biosafety committee (IBC) 222)...5 i, «betes ooo inves e Wem = oe tele iegele rian tel ler ttre 322 
integrated pest management (IPM).......... 25, 29, 31, 60, 61, 83, 93, 102, 104, 105, 123-125, 129, 132-136 
272, 276, 278, 313, 314, 327, 414, 419, 420, 422, 423, 431 
Intensive Plot System (IPS) 5 a. = -e Unrate sate ee = edn, he steerage eects te epee nee ee 111, 418 
interaction(s) 
naturalveneMmys= "Pest Pi Wes pik ls ieve Wleceids ahem teva ora jai, lala a ay may we sae asepea tre ae 102;:105, Liga aes 
physidlogical 2h sbth Aw Bem BOR See ee ER 6s Ae cle ae eee ee 110 
internationalourisni .£%. 22-0). 2 A Aleks ss Seen a a eee eee 156 
international, trades sG-2. AG a A. Se eg ok 8 so Re i ee een 156 
interstate shipments'(U:S)io£ imported species (Abc Ce Pee. . oa 6 canons ana ie ane nee Wine eee 267 
introduction(s) 
harmful «es sc. cabs oo ate date Crew R arene d Fis 8 Mbe ats Ghd S95 Oe Olea eo 8 oo Re ee 154, 156 
of antagonistSWiin Poi i<. 6 dawg ede d. veg ya Sew sede oH Na) ae Na & 6 epee ee ee 4] 
Ofinsect PAthOBENs vo junk) V5 ois ls we GM Se tee eee ae oe ack ere ee eee 10-72,:314 93 157330 
ofmaturalencinies;. «2902s: 6, 15, 16, 18, 20, 21, 23, 26-28, 31,.37-39, 45; 49, 52, 57-59; 6771s 
100, 106, 116, 146, 154-156, 260, 397, 401, 406, 410, 419, 421, 430, 441-444, 453, 454, 466 
OF plants: ee oth Sess ae ws Soe ee ca oe ee 21, 28, 439, 453, 461, 466 
Onplanned*ey Set MES cco e xe sce bo ee cie clots ae 5-409, 8 al lee se aotearoa ea 453 
Pivertemulsions, <4 wisest Ser Sed «tern ced sot be A eee ee bs ee Se ee ee 90, 91 
irrigation systems 
application of entomopathogens with sj y255 © aa. Ske Pe ay esa se tae es «2 es ee 288, 289 
aquatienweeds iis dca. is 2 the 00's edn Hoan gh pA Roem ss cee eee cu One at eae on 128 
island etosyStemsi.. ig ss .gk a VER Sew LS MOE E TEREST Re ORES Be OER RES Oe ot aan ee 466 
island: Hybrid bees asic gue Silo Wo as sa ed cee ee ee 3 eS eae ee ee a 328 
isoelectric focusing (IEF) technique 72.2.4; oo: nace a eee eee eae Aen ec ae ae 310 
isozyme techniques/2g. 70 RS JERE. pod adie Sone ew eo ie sages eR Eee ee eet A eee co 423 
K 
Kedactonianalysis 5 da. Wier fale gains 86% ean ee oa Ree Oe ae ET oe eee ae 422 
kairomone(S) pepe) oa. 3 on ons ee eee ce eee ae een re ie ee ee ee 31, 32, 65, 66, 397 
Kanamycin nytt esse aa Seve Sai Sis 95 a) EN ane toe oe aloes eee aa OSI i, CO a a) Op 300 
KapOwgiehis «sides ob Bo an sig wee od 2 hale oe Ge a Sead oe, ORT One as ea 68, 279 
keyifactor fils Sit. 5s ices ee = Sas egw Hane ee mieveee pis phe scale pie Sob oes Sete 434, 443 
kimase sve PRS eS 6 ohare hen cee CR ae Sele emer Gene care nce eee ee ee ae cried ee att 
Koch's postulates of pathogenicity? x45, facie toe ele oe ee ent A eee 305, 306 
Kocidesl01WP™ (copper hydroxide) 75... 4. Steen ee be Pee ene ee 308 
L 
laboratory rearing/culture/propagation (see also in vitro production and mass production) ...... 398, 421, 431 
Of palasites 4. ua. Gere aaah cep taka cho ee aestuarii 398, 401, 419, 421, 423, 441, 443 
Okspiroplasmas |. ./ ssivhiuiieig ehoriatecy Whe & cote e taanenno wh anita one ree suena acl i tice ee 305 
of. wirusésieee, beh AiR Ge ES Ree OR GREE one agriuachacia aks aunt aac ch ecm ne 113, 436 
land-grant universities, general (see also specific universities in Index of Organizations and 
ABENCIES) susis disc 'in SE op baeay crm nigh nel Moca atc sel. heh ae eet ala ot en a LOD ES! 
landscape plants: # ses 2S oe CR ee en a nr ie eee ee ee 124 
Dar VACCINE MPa de gana it ot's sph tov aepap giver can ph tle enatiolak slpie! coset Rh wlan collenase ey fraves taht oe aL ne 297 
larvacicle(S) osc. sous ls alana: ane @Pesauite supucteen gt hone sched aren vets Ashen Reichl an cae ae iene hanes ENS 278 
Late Kp Sea Ra sis aca slic iauatins <ipemipepe tach Sineer el tocar Green ol Seman Pata LA te of AE PRR oh CE ORIEN Gt testes en 84 
La wingerass(es ) BIR sic. 6 pen coto de pidiied sHagotcea seen oonatin aatae etch es melee oa Enel aN oN SNS 27 
leafigalls...v5: terG Ate wie ee be nk a SAR ste e RS me cece lie rh cotsietee Ene eae 427 
liberation(s), see release(s) 
Life hist yi Bye c.cis sere i ase hepa Wea teagan eg tee ee 396, 406, 407, 418 
life tables Mitr ssic\oj usd cs- Sica autecvsucls, Slesecbdi hang tna sic coe eee fon ack Sa ce ae a 129, 415, 417, 418 


570 


SES). ong 8 teas ayaeetthcbues be ab aly Seele Rute OnLONALRe BTES CE at 310 
PLIES os aces diet diate ahi Sere pene oe Cen tae at te anne ts i a ea 273529092935 323 
Ripracer: ca leT Ave t SAL Mw Neree rn Mee MRE RE Nees, ace ects. it ys dh diaesohwtsigici diol aMreeti ais ob Ane le) uaa doe PORES OSS 302 
TEs eC em Pert NA AM ee! Ee Pent rdirdaly-dukunileha sv iatiBi spmiiakawirced Als a\ sale ava 21, 25, 28/58; 64). 139 
DGB ay ugha 6 Oi Seg DBL Ch Cea ae gn ae 405, 452, 458 
CNet OE Pee mee IW. Besar ee eR Neen Sto a sW. 9,1 caf Soe ih howWadhis wold. es PAG @ Acs SORE 404, 413, 463, 465 
Ey SO yO me eRe eae eee AY A ere Nn edie Givens Saeed aoa Bea x aid eva aidne eR O RRM ES ve 323 
M 
Pee rIOCLIUIN) Merete: aver he ae Rae ew IPN ere Atha ls (iol So Mig el Sed ralals cl god Syaew eva aaah aes 305 
Ree ie a nee eR AE 7 aN yA NBA Aa Uy caleba shcbuacotshardbevnia tse Mahe Da he Wass od 327 
macromolectiar protein synthesis inhibitiond@actor (MSIF) co .t3e6 election ve we. vs JD Ae 302 
TAN LAP Ne Le RT A RR eh oe tty Bo ea Btond. GAS e sel de ae i DUNG a) cts Mined Grated ns bo RE AL eY 284, 294 
Teer AC OT PT IY, See ee ee 5 Ee GE Se ck Se ee WAR AWilalds VOR SEG when mel ee & 279, 312 
PUL aaNet tS eee we EE A eA a hal Bal Sasa sles MA Sd Bai dadee ws 436, 439, 444, 446, 462, 463, 466 
manipulation 
RSC OSV SCI So Pay ACM er Sty a Adhd ut Wah AGED WI ACA Sd hc eRen Wink od dr ann ical ad ahs Wale IG om 412, 449 
SRE ALI A MOCMEINIVE PO DULALIONIS gies MNEs ch ac acctaicl ahah streak beh utay Dh uate ae « 396, 418, 423, 446-448, 458 
COTM a oo ce map sb ch dc Bas aaa atc gos Tt lo ee cae ae Ba ne eS ee 64 
Pe APCLSe ALOR OSE OC ELLE Mee we Ai yeh, 7 cn leet nay ave) ohaYO? anny vo Sh MRMRRE WILTON vetoed elim sl Dl GW) chor of dei ov wllees 460 
Sete INC OGIEGC Gg Meme Ree mer wR wes aT ree er EMS Ate Wee HAVANA A RENAN cel cileye’ ah ale artsu moptusec ancy oN» Sly 280 
Bhinse MUrOUUC On ance AUucinemMalion WONCEptr syns oo aes Stes oer Sis kal ieee SOR Meee aenan Gees 72 
mass production/mass rearing .......... 30, 31, 33, 35, 36, 54, 61-64, 66, 71, 89, 90, 109-111, 120, 121, 123, 
127, 128-130, 271, 272, 299, 306, 396, 401, 455 
CLD ACtEr ic are ree Ree rere. Snr a eet eer ye ee SO. seat he eas) or penned 8 dls lk Shei anon 289, 299, 318 
SRP VITUSOS Eat aie Pa. c cae RS Aah ane Aig Ae ad) Steal As oh eo) EERE SS ye ahs, Aa OAS 35, 36 
CSESEMLG nye Pe as RN a or il aT ich sh MA ARMIES MOT MAO a Ae Sie BE ANT ng ig 314 
FORA SM MIE PO Reggae rey ay hace etd drag os Matias iat Sr'ai has RNP we dl RR Od 31, 288, 299, 306, 317, 318 
PETC TOS DOIG Meee ae eee Ree ee OR TAN cette ne eh kee Rubs. kre ch ae oo rE TORR Slz 
CUMCIIGOUES BEAe Trt A anne 18 nae ad ee tear o! PA Nee aaah ne se es 33, 66, 123, 294, 314, 406 
Of noctiid larvae, with parasitoids and viral pathogens ...2 0262.66.06 i ewe eee wt pee de ee 271 
of parasites and predators...... 30, 61-64, 66, 127, 128-130, 396, 401, 402, 411, 415, 416, 439, 446, 455 
Ci DianupalOsens Raat acne vam en Coane sed Aad added ode edo hay SA ee 89, 90 
SEURY IEUSES GER Oa CRN AIG werd oo nex eaoo es fia! PNA Stee: Sane Hoke Alcaal 35, 36, 159, 306, 318, 319, 436, 452 
MclIntire-Stennis Act, see Forestry Research, State Plans, and Assistance Act of 1962 
Berea mAnCvvetclinary.colonmiOlogyg. ) frwins one 8 a) o aitcta- ded kaa nee See ON Bane sect, ee eee ey AM 150 
REMOL ATIC arn OLCEINCINSis ste er A Ran Pan hee GT eae RLS sts dpe ae eames a SRD Oe 17S 
CPE LOMUGC Ee er Ee AO te ce Mee: LGR. ere IEE Sia ta ok ae hae da aads ERIN 125 
"Metterhouse Report", see also APHIS PPQ Biological Control 
By AIAN HREDOLE Gam Bites AUT Arte aR ten MEO e ERG os Ged a PATE APS Cad eels dene 131 
mice, mouse, see rodent 
MenOLIAL COU OLN Teme re eee cos Te PE Tea dad dae < 33=39,0103,1472157-199, 270; 2719275? 276, 
279-281, 283, 287-289, 308-310, 312, 317-319, 327, 328, 424, 435, 436, 438, 444, 445 
SER LAIC ETSTALC ANU RTE TED rash eens het AiR A pele Sie pe cutee a aie aid @ al Pada wR viace Pus Beg oa cee 414, 431 
Be Ter TAR CCVIDeC mie ama ose s tes > ene Ae ha ea tae hoo dgm se acing SAT RE oye 274,203 
RECT PIUG aes tek 2 sei sive Saum cli as dvaere Sates Mea ep Sa as tapers PN Seta eh poe WD eM pte et 101, 116 
SRR ONC AIN SOM tr eer ant eed he Rene did Nide'anhya o's Reed Wane vases es 396, 408, 409, 429, 463 
microsporida/microsporidan (see also host range, 
TESS PLOUUCTION UNteenny ucatitr scutes Ores ones 35, 277, 283-286, 288, 291, 294, 295, 312, 313, 408, 415, 452 
PINES Lei eet ted ea ces, or allay dena where Yond die Bie Baja ate Renee kere aMMe AEE, See A Gen 284 
UES yt ool LIE 0s SRA Aa) RI ae gn YP ee ar a ee a 283, 296, 298 
re ee a he Rae een ied been eee Tw wie oki 3d was ks Fee RM eels Ro 2977328 
OOS AAPL. coe hace te a ead Or Oe eo ace Arie ee eI cS CCE ar 459, 460 
BMI CAD CAUON aay keys ak Maniac sles ed ee hed ea aos Cea he Eee ees Le 429, 431, 450 
mite(s) 
MVE O Ora MMe eee Sine eis tae ayeroNaehniner cin aie gia) Whaa fon ave n Haims edi Bd,d ata oo x Re 395 
rl NN ate leaded dd ee diee ay? Pr AOS Mes ees BUN. 297, 298, 446 


=| 


PHOPETIC fea eo cdeeaas oss wm ie elelace  daviclyn avabey estilo a nanan da onile py SPDR i Acalate epee yea ee ee 408 


predaCeous) predatory i. jct-rsjctabonok wicunns uss coeseh es <sthslonns sunray aelehen tun den cae ete teehee ana 398, 405, 446 
saprophytic may: Bis semeriey aie ree N0Ih tons sBURE «e Wisiave a ohvu bode ohny a elenoae Ge ok irar ickey ogni 398 
tracheal Boe28 oR, dsiccnsceyivne Aten duh oniieoes eames cnt cote di hou eeOe tora < iki dige aye, ang eae aan eae 297 
Miticides(seeralsosacaricicle) Dave. LI se gee clo cies sss aro) lu shy owes de eepoed td mettanst keene oa cleek hoe ae ea 287 
mitochondria: cade wi tels wlohe css) cae ae uertoacu dhs clei te bvgn MACY Sahay OPaaas Rae GeO CIBWON OR om, Monee a ie are 300 
models/modelliing 4.55 Ac aceretseestacieep edn kits eee een ear: 402, 404, 408, 419, 422, 443, 446, 451 
econometticiers FOGR i od ons aephoakiee ose Wel) Oe oleae wk wt kl ek om Re oere See ele ee 128 
ofthost-pathogen interactions: <2 Ginn. oes vc ae sone, «8 Sie eal sip inte oareein err ee 315 
populations ..sedet syne el eel ae een acpea ke seem trae 402, 404, 408, 443, 446 
monitoring (seé:also aerial detection) 2215.) .04- ee ces os =, cor eienayrs egestas 155, 287, 309, 433, 458 
monhoclonalantibodies oo. c sie cvaceuc a tseac ey ehphud srevey od. A eens DORN ee bola due aye cence eee eee 323 
mortality/mortality factors (caus suas. d seats Poodle. eens < cea ee 398-400, 403, 405, 408, 414, 418, 419, 
422-424, 427, 429, 431, 433, 434, 439, 441, 452 
tren: I: Bh GIP ALE Gtr een ha nai a Ray eee 400, 402, 413, 438, 453, 454 
Multilare 2 ae 6 o dol Wc RG Roe, body Bata Oks Aw ys yeh ee ce ee 402 
“minmmies:Thoney. bee a 5 i ieeas Saw aha ditaete niterssone ley Gare sear es aesscpuvdhay gpa Hel ks yg ee ee p4 be) 
PUSH OOITCS ) re ee He ME sacs, sea hk Sey acacia i sa ceaptes tv tele, apn ied hsp Sheyos ey Bk RRR ee 458, 462 
Cdiblekeg aed 85) on os, oars ee eR eg ab ee I a ee oe rte eee 462 
FICS “cs, ace SRE ERS LAM a SI Se: 1 AOS 43 aS a. eee 67, 68 
Mutagenesis | a. 2.24 Swe wh shoo scape Lassie cinwie dol hers, Slals, desbenstece Pad eatieneie os) ae ee 95 
homolog-scanming ss. 5 aie /ssisga Ns, salts 94 bins ah sash alle nella) ws 9, © COANE oe it cn ea 432 
miutualisii (es bi POr. ce PE ks So thee UR RE Be RES ws. ee eee 306, 408, 458 
Mycan at eae nbatege «Quite ats s PEROT IN ois wi deeeih y igs 1eece Micon epee kerne ogee ete ee ee 287 
PAY COpHAg Vikas zrrtaheaaa nae Bie, Is oye 8 dan esa a, 93 Sethe nat Saar none re apart Ode a ee ee 462 
InyCoplasmasypgcep oe co: dete pesiech S30 ges Amys ahs cto hh gee cing Sete pale) axes Sn eae tk gd 9 a 305, 306 
role.in infection by human, immunodeficiency virus (HIV) 3.55556. 05-54s cae den,u-as-s eee 306 
mycoplasma-lketorganisms (MLOS) (0.05.10 500 age one a eee es ee 306, 450 
DivGosis G Sanne aac © S Mak etes we ontpes oh tow Seegeitn a thay «Gane hike eas eros ew acca tk ofa 275 
DIV COVIFUSES TIE HO LE 5 Sad: Aun eal pant nyt tly ae 9 omeecn a eh cea cel alata, op alae ae 456 
N 
Neacetylimuramidase, ociiais'og ak ue aon hu yee ea a eee atediorae« 56h Sat acest ad 323 
narcotiqplants @2f. BAe Rt RPP E ono s nr honaiy cite teenie urn a ee eee STO | 
"National Biological Control Institute Implementation Plan", proposed .................... nite: 133, 143 
National Environmental Policy Act of 1969. ent .ro as am = gas a0 ee ee 75 
natural areas, classical biological control in’. Wy sa3 «saa ais ac nt ess pa cre a by 
Natural controle. 296.2. see 395, 397, 404, 406, 407, 412, 415, 428, 432, 434, 435, 438, 444, 445, 466, 467 
natural enemies 
eXotiC WGA Actas ut ee 120, 123-125, 130, 145, 146, 148, 260, 395, 397, 401, 416-419, 423 
INCIVENOUS is ols cy Sri aces Eins One Sew PR MONE pn ew aise ae OS ee eae eG 2s ee rr 130 
Native ME AP Lk BT. OP POs Pee a sn eh ee 260, 395, 397, 401, 402, 404, 406, 444 
of nematodes: .ied hs GRE Gs Leet Bee tee i ae a ee. ee eee 12 
OR WECS iia 5: hs. aan hte oi oreac SRL a Rae ar Re ee ck ER es ee: 25, 36, 37, 466, 467 
navigable waterways jos 6 ois/se ao das Gusmw ea ang alent sorte so See Sura ac ha, ap eee er 38 
NBRF (National Biomedical Research Foundation) protein data base ............... 0.0. cece eee eee 31 
nematicide(s th weiee seen ae ek ee Re A eee 5 Sr ee oe 12, 22, 39, 40, 91 
nematodels)ikus 2a sisacendn ea ee 19-22, 33, 52, 57, 58, 66-69, 72, 79, 83, 84, 91, 92, 102, 116, 148, 164, 
260, 264, 395, 396, 398, 401, 404-409, 412, 413, 452, 453, 456, 458, 462 
application with.commiercial sprayers a5... < ac 50a utes na eae aren eee ane ee 278 
arthropod-parasitic a \2 6 enc sa tei Se) ee er ee eee er ae 10, 19, 33, 164, 316, 396, 398, 401 
“bacterium ‘associations... 2.) 0 0 areata Ws, oaepn se nae eee 20083 
CLOP POSES seh. sits, ase aft aan ols cai ay silanes ebale eigen waite Seater tad IM Crea ire ran ee Seale ch ea ek 40 
D1 36 oe gu Sasso, arapeue States aden Sap eae g MAN let aR nade td sc 33, 412 
delivery:systemsiwsnd ss sails Siow Biba 25 cry ae Sens Goose ele eke Io a ne eee en oe glen 68 
SNAOP AL ASHUIG) 5 gos sh say ewan eas wc Ss eee ee ee 395, 404, 405, 407, 408 
SnOMOpathO genie zis, sotiche ancora dea yet eee ed ae ee ae 72, 277-279, 287, 288, 316, 413 


Bye 


SEEN TESTOR. 05S ORG Bley ony Mee eR Eig 52,507 


ae ee ALAS LCmanrn Eee ince Fed « ak Gea Here x wa edna oes os 11, 33, 58, 66-69, 164, 278, 317 

eos ented | RAN a eR i ee eee Ata 2 iyilh araie. Sokttategeh @ ae.G Bare vse’ ped ae « s Wet Sto aN Sad 123,128 

HISTO ERP TIES Yh ce cialis CRAG HERI: CREEL A MP a a 33, 66, 294 

Fan ODAC Smee Reser een ha aan Lo, GPT eG 6 = Caley a bh eS ee oo eS eee ne,'s 456 

Arta eSR GRA sIt Cm mt eet ttn caeierie Nakano Geta Ma Gian tas 13, 101, 102, 108-110, 401, 404-406 

Paso naCOUSHe nes, . eee ee ne een ene we RRR SE i 2 8. Gls 4 Saab aw tee aeba eslels 164 

Dlanveplatt-parasitic..c ee cdenes sve. shes 12, 13, 19, 21, 22, 33, 39, 40, 58, 66, 79, 83, 84, 91, 92, 164 

RRC OCEOUSEMET WAR EE ee Leon cect roma sek tgs 6 So e.s. 6 She cally aw WIG ams see ree 12513,40 

et aC ee ee NS cee we eet Rey ce Rs aly 5G 6 dia.cs, ac one 9 Gob Metoce aon tee hehe, e 13, 22, 462 

eres TEN ei) Fi tS rae eee a eer ee ee tPA asl oh ice <a Ge F siege bots eis eo gas eee, 12, 40 
PEE RN Sheth Slddy olateiaig escuela aolonntan & rece ae aa en rey 219 
Petals a) Co Rea Wey htt) tls Wa nants 2 aes o's Se hh ee ey eens phe oh ems pte 164 
PISBUPIGI ..0, x! a Sens BASSAS Ss cath Sts SURES aa ee ne 300 
MetEe Cee ARO OTIC TI ree men eee ON NOR ey Cet ee A ae as le dae ween cia sa wieinm cd oly ts 123,128 
SOIT OSE TISRCS os ag 9 cosa ke Siete ery Sob AN eae ia uel coe a ey 300 
URED DESO TTAUTSTORD 9) fps ie Se es | Se ey Oe iv picks eRe PCr on a ne 408 
NT te ee CLL CUALY ) Paea een are Bee ee ee Pere tats Genta ate ere apo, Koa id a ldap ian nde alld Nees ahedogs 452 
ere teree retiCremGUON (LO! Ou DCAM SteiT) TOU ee eins a ia Aaa ae Som egg KLE to ans fo Sadar uh Geel soe 4] 
Pee EB CLIOUISES EC CICS CNIS iets Serial ce rene SW fers. Ae ose oy nim SERS oS nln oan sv ns Sha. RRR 154-156 

MOE TIEE oa ae avs hous Bg aN CEO OS UP cic lesa a aa) eg 154, 156, 157 
non-target organisms/species............ 29-415 103, 106, 107, 112, 130, 153; 154, 285, 309, 428. 451, 463 
Notinsamerican Immigrant Arthropod Database (NAIAD) 2.20%. ... 2.52 Fo has wk eo oak 05 olloieeane 155 
North American Nonindigenous Arthropod Database (NANIAD) .......... 0.0.0.0 cece e eee ee 155, 156 
oteew ea lOwance (TOM) So Palent CLiCl) eta. nesta) awn ag «cst «palm Esainat ataers » 6a a ea 8 427 
APRS RLS Sys ye ae ee eae a EA mee 2d 22d 
REC ORI AG) MULSeT) NUUSH Va iar iin Gee ncaa tls Ware Ge aales Dune ae cio 3 124, 288, 413, 453, 456, 458-461 
nutrient 

NE a) Rat ee a yo ahh oicrel o a ihn oes WL ine Ses 'n 9) p+ bie WSL hiv a rap tha en WE 413, 458 

POSEETTRSE oa ho noo Se QR gee BR EEN CEC eR PNRM 5-8 Ent ee em Ree a 458 
nutrition, 

CHET OARYSS os Ou he: dr 2s Oo IA 273, 297, 298, 326 
REN SMEMENNUNT Cor oF Soca, is dionaw Ses ois a 5 p88 “oH eee nak gy MaRS AMET teed SOR ENE RR meee ny 2 276, 279, 280 
O 
SURI TY DK cs ae te ee ese Nai ne io alr ts sie wid Gis ONG. op alw ab hs ap mace he 36, 308, 310 
ER TOST ISTIC ATES <8 SD aS EPS OP! OB ae a eee ere ee ee 304 
SATE UECENCASC SIL ACC ICS ma eres Ct aie Rute ater Ae Siem ah Oe ws pines no) a Re we Siow snh,s Sogn adamant, 123 
EN IRS ORS Ss AO Bee gee a ene ee ee ae 93, 461, 462 
SE OSLER ET NETIC RO WSR Bg Be WES BRR ak Geir 2 ecient gpe ar eee we Bee Sm 324, 455 
LETS TUES TNT. NET area ene rr Pa ae 60, 94, 123, 124, 162, 413, 466 
tag Os or a a we ae iss oo ad eS Wd Ree Hao oS Silane tee ealara eee a ae 425 
Perma MIOLINSec’ NEMOLYMNDN eae swe ale © Siew jes a edd > eae ea aa o> Bao Che aes hs eee 301 
outbreak(s) (see also epidemic) 

BARA Ct MI EMR nk ou pe lon dots <ycinle 6.60 = 09) Hs vt vines ® Sin elo s ga fo oly 6 aon salen 415, 433, 439, 441 

ARSEOTRED” ough cid age ee ie ee 75°28;62, 102103, 105,109. 1.10, 


312, 396, 400-402, 404, 405, 407, 409-411, 415, 
416, 418, 431, 433-435, 438, 439, 444, 445, 447, 450, 452, 453 
oxytetracycline hydrochloride, see Terramycin 


P 

P-32, see phosphorus-32 

parasite(s) (see also parasitoid and nematode) .. 100-106, 108-117, 164, 260, 264, 396-405, 408-413, 415-423, 
427, 428, 433, 434, 438-442, 444-447, 449-452, 455 


ARACEAE Sar fag cine ue crews «nde ayes qj nhs ais we ig ones 108, 164, 330, 331, 416-418 
Set ea Re ee Palate le Meus NA ER allen Peewee Af b's 0k 8 Wis cae © hulbbidue, duwhndanec® of Gah 427 
See en ok ROME eg 8 aig cle uasaalale tub a Mae Wits sh unddi bses lana ea wh abd aed ls 419, 446 


SXOUC 2S oe cet 2 Real nore enh ee ant os React eet 101, 110, 417-419, 423, 439 


external’ gre eee a Se Cae es SF ee ee de Ok Ch eites aeee Pame cn ar ee 440 
extrarégional <4'.¢2 Vis ei ed a5 soy Oeics ete ay ne ace Sees eee aioe a ere ete eae nr er 408 
BreGAariOus® vss ever VN Les te teres Manag © Se ts kate toe One br ete RU eric er eter one oc mene ee 421 
hymenopterousm yn ce ie eee 113, 396, 397, 401, 402, 410, 411, 417, 421, 438, 439, 444, 445 
hyper-, see hyperparasites 
interaction Of Bt with ssc. Uk see ee ee te ne ee ener rer eee 420, 428-430, 450, 451 
internal Os se es ee ek aa SE ET eM Le ae aie ee nc Ron ATRL ene ements oda Mg se eae 405, 440, 444 
Introduced eS ere rie tne eee oie ne here ne orn Renae 410, 418, 419, 438, 442, 443, 444 
Ficecda [11 | 6 Se Maat SAME aa ured ied arenas ania acai a bint Sci ichonreacibis ead) asp say « 276, 294, 295 
TAtlvers Pt rr eee BAe Ea ke ROLLS he ete Ce orc te sce ee 397, 401, 402, 410 
primary ris ee Pee ae Fa Tee orgs ek, eee tee ce cen a ete are ee 419, 440 
SAWhy rae  e ea as ae he epee es or A eee es age See preteen 433, 438, 439, 444 
secondary, see hyperparasites 
social tify er ees ad oa ee lee Pe Ses oe eS oa BE Se ee ee 285 
Solitary ee ete C2 Pee ed Ee Be ee ah ie ak ee ow SAAN aN 419, 445 
parasitoid(s),;see also parasite(S)/ 2.7 sass eee eee see ee a 4, 271, 288, 289, 291, 307, 317, 409, 445 
parthenogenetic/ parthenogenesis": <0.) Pace Cede or ee ets Pas Sten eee ee ee oO One ee 453 
PANZOOTIC’ Ai £0 PE ee Pe ee ee AT seer as fle eis A Stas reine ORT oere cae ane ee eee STZ ate 
passage level sii. s SR SS ess vas eee ee Ue ete as Ree SRO gaia Ett eat cee ean 437 
pasture(s), see also weeds, pasture a7 1 ce eee ee ee oe ee Oe ee eee 299, 466 
Patents fe er me ne toe sR ne eras tate Aine RL er eee 280, 300, 304, 307-309, 314, 323, 427 
pathopen(s) (aos coeds giles Ve ee ee ok ea eee Pepe” oo.cre pen ete een ae cere 264, 299, 455 


arthropod .... 11, 19, 20, 23, 25, 35, 55, 58, 69-73, 163, 164, 271, 272, 275-281, 283-290, 294, 295, 298, 
299, 307-318, 321, 325, 327-331, 403, 408, 413, 415, 419, 422-424, 433, 435, 445, 446, 450, 452 


bacterial’ os. pe7 sess ie oe 7 TIE E ad FPR AER Cy hare coe Chee ee ey Nee 34, 36, 402, 414 
beetles Fe er ee Ie ee oe Ce nt ie ete OS eee Tan E'S GA Een CANCE eae ne 35 
cabbage: insects; ‘control with 224% <s421522e.405 < seeks seeks Cee eee ee Se ee pieced i 
Canker’ 25 See MaCa caer ole ees fs oO ee ree Rene oan iy eee eke accel ccs ne LOT 17 
entomo-, see entomopathogens, and pathogens, insect 
foliar i oorse.c g3 rks ba He Gay ak role eee ae are act ne coe enol 41, 93, 96-98 
LOTESC Earle nevi eres cee ee eee ie Ce Ne ORT noha Een pe Rg Sieh et 100, 101, 455-465 
forest insects“ control. with 2544267 PACs Mee eee ee ea oe al eee re ee 101, 102 
fungal Vee! 654 Lert a2 kA eG eee ee ees eee aes A ae Been 158, 402, 413, 414, 433, 459, 466 
BrASSHOPPEr As yee Pe ee oa Ne eee ee ee, IN Ter Is oh ER Pay Rayer a RUS SNES dy 35 
SYPSY MO We fos he Cee es Wye eae ean One 6 aS eR Oe Oe wire ea mem eee a 424-427 
Honeybee werery Fee Pee ee Aes Gere ene ae tei 4c 11, 34, 157, 273-275, 296, 298, 300, 329 
INdIMENOUS!é 5.4 PRES TTT RPE ie ee eels Ameo Oso ndee tn ERR eR cic te een ee 415 
msect (see'also arthropod) 42a) Vie marreen ets oe te en eae ee 25, 34,52, 04-37, 0645 1Ou 
MOSQUILO? Lie NL es PE OES Seen Acne eee mee, ere meee 35, 71, 158, 159, 276, 283-285; 294 
MEMIAIOdE™, | Be ies eee eee ee Sie TY eS SCout nae ie eae Ee esl ee 12, 13, 40, 91 
plant(see also weed) aa tie cee oe eae are ee es 13, 22, 40, 41, 45, 52, 58, 73, 93-99, 158, 159, 260, 264 
post-harvest’; £02 2054 Bird BES hee 5k eee seen atin er ac eee te eaten te 93, 98.99 
protozoan 22.5 Sies tls oA Otis Se ee ee Oa ee ei ee ee ee ee 34, 35 
TOO" — amen Liens Lee oe 8 PEO rcd Coe ens Rene eee 14, 22, 93, 95, 96, 102, 104, 105, 458, 459 
soilborne Sep Fat ee ee ee ee ee CaM See NTE Cette on Ee are ee oe 40, 41, 89, 93, 94, 413 
TOOT a. take Cag VE Gat eg oe Pea eitee Preeti eanen GALS, Sell tin alee aescre ee RW ORGS ate ae 402, 414, 455-459 
Vital oS 6 oad Baw d ee taw ane oo ate Som ola d Mer eeh ote ean enn RiRnen En Mise Nene ted eet enn eee 158 
WEEE oi i kderddles wah ple 145 ans ORCI Aenean ee eee 58, 73, 78, 81, 83, 87-91, 466, 467 
pathogenicity" 2 2). Sea feet) eee ee PR EUS ee ee ea  e e  a S ee) ak 435 
of aphid pathogens ©) . 52344042 54.4 San a eee Ope a) ae be Sls ere ene 330 
of bacteria 22 °Fi4", Bl ons wee tase haa ka tee eed Caer Race ve ie ety ok ROR ee 328, 402, 429 
Of Btes eae 218 oh pce sale eae ee Se tae ie An Ere ET TT One Tee nek 429, 430 
Of TUNG. cies Sorc ep st Ek Oe Oe ee ek SCO ae eee ee on ate ee I ee 328, 330, 402 
of grégarines a 00243 oh FER Ee Spee eA ee Pe ae ee an ee eee ee S17 
of microsporida: $22 i445 Fiat heats. see Bea ee Nee eee ee eee er 452 
of mycoplasma-like organisms to their Vectors 4%" 272-5; sce nee ee ee 306 


574 


WIPE MOOT SS «sug Ble antsban Woeh airy SR A NAA 3i7 
PCOS al Ite cere aa Lasers eects Pa, ase he kos Wh e's, 4.9) 0 tenets wg Bd eel Adlieoe 9 om 328 
Sr SOs er eee ee oy ca Rid dha vee hb wee Sie we 276, 279, 295, 435, 436 
SCHLALINUL ASP Alin AEG) OPE ME Ce cle PINE ela g sas, Seas Fx ss} vata’ bela aletiws wate e apie 3 114 
proof of, see Koch's postulates 
pathology 
TSOC Le ict oh iy 20, 32-36, 45, 55, 56, 69, 72, 103, 147, 149, 157-159, 270, 271, 279, 281, 287-289, 
296, 299, 308, 309, 313,315, 317,319, 3295330 
TT, 2 9s, othgesl aay at eect I eR Ueno ye Per aurea 39, 40, 47, 76, 93, 94, 98, 147, 280, 306 
oe eet OIC ee Nee ee Et ee eng cig wae diy. tae Sig cocn 4 och ens ip wise we Mele, ereps ons 463 
De ON ret eee eae ree alse es clark Gob las + lac ss dae Se nace a4 6 #4les wel on 301 
eUrNCARVLICy Mere ene ee ete MERE SON Soy y elehc en tht ceca baie dieje laa ca 6 shoe ae 43] 
permit(s)/permitting 
POTASH TROVE “sw aie leche a eile thd OER Roi oer 2 a Pra PN 27 268 
HOVER 5g @olbd Ou tele Beeler eee ns ks Ar sor, Se a a a ee 268 
DP SYS IAS GEN Wey RIND. Sg a Sh ie ha rR 309 
VORA BIOGED 2. ose a tatantieeiy IARI ARR nega Sipe ome Ula Near ie ne 285 
DYED! athe cr 6 BRS nce Gatun Sune th ge mER ICG SU aa Seed ee 115, 430, 450, 451 
DRESS G2 5 0S ts a chal: ROR ORS ao ear Eee ao 321 
SSA VE EY ACEI mA reed TE ey Ws cea oc SRGS, ay sa sas RMENS Cau, Seg ba ara aa! 4 4s So bee 278 
BR UNEIRGE) 0 pio aad eetaewes aaa aah Bs Oi ek eee Pe 104, 304, 319 
pest(s) 
PUT Sp OIG) 22! of SUPE RPS a Speed ey an sie, noe cers NS ea ear 120, 137, 148, 153, 164, 165 
SETPSI IY gnc ondelip SSRN co ROR SO ele 4 A IG a ge re rca en 77, 81, 86, 165 
Gi SESALCLOTRY 6 0! = oh Shes cea Bet RO PDAS) Si DR ep AOI GRE ESRI ree) ce ca a 126 
Cla ICDTATPNCTE oo Cah: 5 pel del ane amis oe WA a coe eu ae Ra <5» fl ng a rr er er a 126 
CEMCNVS ayo, eek wteheluty Selle RR Ree Sl AT lr aR I a 148, 156, 158 
HOPKIAE cbc e due Gomis ile i erat gers a8 pe SA ge ee a 150 
Rs GALE att) SCC IN TERN PT erect aries een cct ee, F oaie «NOR ave dG mld 4» Wit.d grate dial capita 147, 316 
POREEUNIOOUCEC frye ret en aeot. Saher nee a Mey bio «is dae 101-104, 106, 410, 415, 416, 438, 439, 453 
(astbe CVT WETIGA TITTSTEN EY, Bok oh, lag 6 Sea masta io,) 3 hcl et 64, 72, 158, 159, 165 
ESTE TT ATRTS, cooe cgepash gosta > Se sea EveN Aes ie ee ee 12451265 133 481355- 136 
SARE CREW osc «xe copies ratte ete getay ge ieee gray ele aoe ap 278, 331 
DOSE IGEV COUMMME TRee re yates Sine eae 6 oles Sita aie 6 sa lew RN ek a ayes sO se en 47, 69, 93, 98, 99, 165 
eT Pt ee een er ene te id Shee i gid Oh adios Sieh es eka wea ak 33, 89, 92, 94 
TEMEEATY gic ai 0 theehlaShaed Sie ued ne Sah OA SANE iene aN a ea ara ier a ae a er oo) 
Perea Ate (USCCE) teen te te rene ee criete pipe aie sue Re nis a Sig 8a 9 6 dew oe 147, 270, 281, 327 
TEESE 2 iuyak otter woh elke’ 2: 94. APaet ear Jee aR ys 1 aga reg Le Nee Pra eT Ore 90 
BeeSUSGHIC( S) eral. ecs> : akey- 23-29, 32, 42, 122, 146, 159, 273, 300, 414, 417, 424-426, 428-430, 445, 450, 458 
eat ee ee eer rere tee ating Pei Na eens cue eos e ee nec e Ohm Rhee wate 428, 429 
FMESOT ATS see, < po hemeeet a ne dag Baty etn SIE en aU 298 
SRE S SCC Mee er ee ee hg ctr pty singe eae tiny lay ds 3 8 5 e+ 8 dak cme ee 103 
Sore ates DOctr I ey eee Re tN celia ak eb iapenkeg Ras AE Cae aide ea ys ew 23 
ig RPE ES Oats ES Sa eee ea ere 23, 31, 102, 107, 159, 309, 319, 330, 424, 425 
Pree oiverita vec Ominatl Ole meme ema eis fe ae eters ean! alia te Gud els woe o che 8 otra eh are's Siasouae eras 424 
PC tee rn oe ca crs itp ev ea ee Os 20, 36, 70, 159, 308, 309, 424-426, 430 
Or Ree Pee oe ee nn ose ae sy elev dal dad wane Mee eased Otome 309 
Or fe ers Pies tae ns oe Male We eae eae 290, 319, 323, 325, 459 
SN SSSA oy och £5 So BR alk Eh 8 cee Mee ne Fa ai era Error ioe ee oP 427 
PeMeTOUMIC( Sime eg teen chic sas <u wien cue. 29, 69, 102, 103, 108, 109, 328, 397, 402, 403, 434, 448, 449 
SP TRYST ETS Ogee cos od ott RRR epee MPO toe a gene en geo Cra a Ree ea a Re ee 403 
NO nee ce ea gir te ie wie niga anise ly are bie Spe aa wes « 306, 407, 408 
phosphorus 
PPR CEvUDY IAMS ert ie ar he ee eee os Select te eyes ees Siena lt: 458 
ereraIAr Kite OL DiCy) Maree RN Cs rota cies ers wars elk roe Gin «atk ipa Nala 449 
eM Gs i ere de ee ae in Ae one mlh Baieie he spaniel bis falietens 423 «oh 97 
Fp VPC RTECER'O” yy css 9 at a deg Bk 9 ARNE Coan ae cae 90, 98 


physiology 


of ectomycorrhizal fungi /. 25000 G6 soa ae at a ae ee ee ee ee ee 459 
nutritional. fo"... ck soe eee a OT OO Oe rae 407, 452 
phytoalexins 7... e302 os ok oe Ga doe pee Sig eens Soe ace ogy wee epee a ee gee ate 96, 457 
phytophagous organisms «34.2250. 500 62 4 ate vee be eras «Oe oly 6 eee ana ctrte aa eta ee ee 268 
PhytotoXin ssw viGen> cance dupe et leisy Whe sisiGas Waa, do sapl sere oenartag singt dias “uiatcake uch iNet Car ee sn ee 96 
pigmentation." ./4- arco: 55.) ecu musns’ Sages caine aie See acs aie © Gn came eee epee ere an ee 282, 320 
PINOleNe F167 4. i oe weve. ace ope s tyne mle OU oe 8 Sans ca ley bud eel mee Gt le Sag tne ee ae a 429 
plant-fungus cultures 3.5. 0b cs ce beds pee Cees hone ee no fees Crete enna ence ete Geert 459 
plantations, tee ss S20 08 cane & cee cts eee eee eee eee areas ei 410, 411, 413, 414, 421, 454, 460, 461 
plaque assay fy.0.00e.6 5 ca daes gee beaten eee wi bas bos ce oe hs mia ee Gedy eee cme attee oe eae ee 271 
plasmogamy = ii. bos sas os ka eee ced ha bea ys eee ee aero ata ok Seon te erry ornare a ee 295 
pneumonia (human): 3.28 sec 8 S255 de OR ee en Sa eine Relate Seles eee nll ee ere 305 
pollinmator(S) yy acer oe nse cir ee ihe care ean eel wie me ae Gn ose Sh eck tne ea 156, 325, 326 
polytlavonoid | ..c 2 fai ex css eka ne eee tees ot ne ee aige bie Oe beeen teen a 309 
PolVinediaenc nee wu ke cree civ eae net erage ers ache es eeee ter epee 271, 280, 282, 300, 301, 319, 426, 427 
polyhedra derived virions (PDV) (oe bas ek ent oh ys ee nee oe te eee en ee ee 301 
polyhedrin gene... cts gs ene coun nee g We ue AES Reaeerd es See sro ONS EMR RS et ee 311 
POPVOXIN(S) oe u.ic.s sh eis epoh otek & oie be ernie oOo caer Shokg ae Oia eo he Gale eee Ue eee 463 
PORVOxI De os Sto ee untuk eek eee cok ee eedte te oer ne nc ern eae cn 105, 118, 463 
polyphagous/polyphagy™ Boece... fe can te wake sooo k Shee 0 One eee ore ee 434, 440 
Population Gynauucs me new aue tee ee oe 102-106, 109, 110, 112, 114, 115, 286, 287, 401-404, 413, 417, 
418, 420, 422, 431, 433, 439, 443, 446, 447, 449, 451, 452 
population manipulation so. este ee ee eas Cee ten Gen een eee 396, 446, 447 
population models/modeling, see models/modelling 
POpUlatron TeSubAlON ye woe ce nye oan che eae te eee eee te 413, 434, 438, 439, 444-448 
population structure 
BOTICUC eon fonda eceraral aaa 04. 6 doh a is woe aa ne oy tease ete yoke Oats tone eee ER tec ane ee 423 
PODUIatON SPDIeSSION <2" Gee an eer ee ee Ae ee ed 401, 408, 410, 416, 444, 450 
POTASSIUM TOF cary cne ns cde n ee ott We or ee ere OMe ca, eS ch den rn en 431 
potency 
(8) ie 5 lath Ne eli at tA Mer AU ee Mater § Sa eS eked hy APM ye dy Ey Es 295, 320, 428-430 
OF VILMSCS tee tao eran secs Cece Sinn Ne ee Rete Ge ee re he ene re 304, 426, 427, 436 
POUR Y er cc sis taue epee ns ie bb me esa gone detae eiehee 2 Macnee de, ce Rigs a en 64 
PIOGSHON ree 85 nas cae wae ee aaty © ore gts eine alter cae eV: pate ee eee ne en 108, 448 
QMS cima g nya en oe Saas faite wae 1S Ain we epebe MMR ne nue mr ore fe lalrauec oleate oooae ine cnet 449, 450 
ATLNTOPO 4x75 ven store. wi + 5 chase ait a) ele 8 Seamer evi eg tn ec gt ge Oe 398, 399, 434, 449 
DIT uo cataree’ Saseas Ganik® gaye aie erated deienaesiete, ce ataeht caeg eae eee 397, 399, 400, 413, 439, 449 
Dredatn(S) ener. ot ee eee 23-25, 28-32, 100-110, 164, 397, 400, 401, 412, 416, 433, 447, 449, 453, 454 
ADDIG ras Sites oh a ohh G Sine Ute ns oo ene Gholade Ga ed Ge Gn en 124, 129 
ATACI ME 2 50 ss Ge re whe acta yates me Gene ad 0 rte on deer ne Oe ne 105, 113 
SQUTODOG soc te eee 102, 108, 112, 113, 115, 116, 164, 260, 264, 271, 285, 291, 307, 309, 329, 330, 
395-404, 411-413, 416-418, 420, 422, 428, 433-435, 439, 444-450, 453-456, 462 
AVIA erakire few: cee here te cee eee 101, 105, 108-110, 113, 115, 400, 403, 434, 446, 447, 449, 462 
CIpter Oye oe co seit ae tes utuete 9 ie ole els te petted chore is Rina an Oe ee 397, 401 
CUISEPIGUCHOR Ol s. wlnena te ee cee ee ee Fa. oe) Mal atelie at Se ate salt Gorasre none Oty Re ee ae 398 
CU (gi ea rer Pe Aa ah DR MC tor Acie aint ANAM Aee Oa, Pall Be a cil 106, 110, 148, 395, 397, 401 
FOUTIICTA Fs su on wee ae eu shee ee Pore teeta eae IO te Re 105, 446, 450 
Of Torest Pests” e205 Go ee ee ce eee nya ee ee 107 
INSOCE 9S woe us site Ske ae ae eels wpa ete oe sigtatecre teat eet et a ae er rr 113 
HC 1]: oa eA AA WARM MIM ALR EE Fo Lae Cc RNs ee 116, 448 
iN, ie ee a eri Ce Amn NA Se Raa A eel gm ea ee Se 395, 397 
PPTOY FALIOS 605 eran vas wats eta a eta at alle ees ale eA ee a 30 
of tree pathogens vai 6 T5705 a er eee ane ee ee 455 
vertebrate 6 106i is 3s SE eat te pe ataee ett St te ea 447 
preference, see'also host/prey preference). 40 ee eee 403, 407, 409, 412 
PIESCrvallves 0s, ca. ae whe oe bates Gene een nce energie ee 326, 463 


576 


praaeandusiry (see also commercial, commercialization) <2. 2.5 eee eee ga eee ete eens 437, 462 


DE ENOTES, CTSSANAO USTED, ©. gh NO a ee) 0 ee a 464 
OTIS I, ES Boe ny cae et Cm Re ee 465 
a re I oA A ed ea Se as scien afiag | ge finals 9 /6) +4 HOHE Symi 'd 4 vod 4.6 Gow kT «AOE 310 
een mee Ir Pt ee BORE, IE Me ae Gaus ous Tosyiys, aces anne tog yernisaue yg 8 Side end me ee oi ee 432 
aD i ee EG Pa EAL hee fats “chesbbc. dyicnys ety pags’ age grin, done ee eve wh 4 Cas BS HOSA 43] 
HEATON os oa Bcopa tion le BER Sat eg IR 311 
ASST ay SO RES RRS er oy ee Pe Oe 431, 432 
protozoa/protozoan 
Beers ITEC ALTO SETS) PLAS CME Mer ern Rr ie Batis tg ior i's Sony aie eis 30; 9) ecb syceavarnse, vadve ous sade 33,159, 295 
parasites/pathogens ........ 34-36, 158, 159, 274, 276, 277, 286, 313, 315, 317, 324, 327, 328, 331, 452 
taxonomy, see taxonomy/systematics, protozoan 
THAT ORS co ue ge Li iis Sp nd EOS oe On ree oer A 
ih emma wia SO (PU 400) ori laty sh aiiepecerfcehe sities 9 406.8 25, 46, 56, 80, 82, 101, 111, 116, 151, 410, 417, 453 
Irn eR ENE TUN rer os etal ae led sce 8 154 6%. ons ans, spabs Fh aicde dane. apapa eiace sen wd Rae pp eS 463 
purothionins, see wheat 
Pare mCOdy nOn-InTeCHOUs CISOrGelOt NONCY DOCS). ogc cscs fe atts 8 pee de bP yaa we Se yk ke ee eee 297 
USUNTTE VS Sucre copst seat AA RR Sie Oe aa ar 272, 319, 324, 455 
Q 
a iimeaa ne Waid Lin yaa SSCSSINCO UM oer tant reais a isicSe says Sn es Kees 6 aus eee ne 68, 71, 123 
OPER TIO Vn oc Os ae or 24-26, 28, 37, 39, 44, 52, 54, 56, 57, 59, 74, 79-83, 101, 106, 120, 
124, 125, 132, 135, 147, 148, 150, 153, 423, 443, 466 
OG a a de eee chen se cared <Eet cal Ch ates iteay 6-H) Se ole Sosy. 4/08 9) @ aig ab aciede UBhses'e 6. poh iaren ea aaa Suey calle 120 
VER IRA ae © a 1M Ney ie eh er ea in cnr eer ieee oe 45, 49, 50, 52, 53, 56-58, 75, 78-83, 88, 101, 
106, 148, 149, 151, 156, 157, 262, 263, 266-268, 419, 421, 423, 442, 453, 466 
R 
RAC, see Recombinant Advisory Committee 
a Ar a MO PMS at ATEN Mca heh ak oo ayn, 0s) 9 wg celieie aaa O.0 # Ge tw gale wl woas'w acd Saga dips eb eed 41] 
ene COO MLEAC SL Ee Oe EE, Fe oe ia Ser ares a olen ses g lessen ah eray bias 8p 988, oan, eno than pilin nneetiegaeens 449 
ey cee Se PRT ele, iy) red heecs sco aie di vvel ans ie eo eh eevee Wille a Sn aoe & adla-o o Soman aM A Role R77) 
ce SEIN SORSTOTN GI ho ss as Sy pa leur Se OR nn are 313 
ranvge/rangeland, see also weeds, tangeland 2.0.06. ...0600. 02s cue. L224 1302162, 3 123.133 21-3330 
EAeIENCTERSe (MUNODU AON CyNAamUCs)\.mukieee akticis and othe sve sew. atts Gu ale waved Dew eae es 404, 418 
eee ee eee tet CETERA TRS CCT Ge occ psa os oka ws eesidl eae bis eo 8 win 8 # aydyecah w © eee tee ales 432 
SES TPA (OSS ©) CM erento Ci aay al) ee ee wee Pie mee ea ae 50, 79, 454 
arr aire] VIAL CUONTMIILECO (TANG Orie aia Peri ateat 9 2 Gig 5k" aie oiet ielGs acersaam'aiat soe fad oll ck muedeee 322. 
recombinant DNA (see also genetic engineering, and transgenic) 
COCO DST BE ou La WEIS aS BION, ConA rae ne onan Ee ee 322, 324 
ese Sr or ogelce ep el taaaV fede 4 6s Wi9.9 ys ale mu tie ym Slee moma ele ona 95, 280, 321-323 
mae aan NIT 2 AOS S asaya dhe ois eh api chalet sai renis rs ibe sions, 39! nada, dca di'e 6 eas 124, 127, 130, 419, 437 
redistribution of natural enemies (see also recolonization) ............... 0c eee ee eee 120, 123-125, 129 
Oo LEOSRTNTT: og cok Bn yb AE RS On ee re 460, 461, 466 
registration 
ee ee Fa ee atone 2) ei rititah day shiny va tan ‘lie Pej "soe Suave es 8 ese Ste 126, 127,159, 292, 299 
i a OE el Se cis ehh « Aa do ody oR ay PTAA Os My Wise», #1 Qe, Scams 292 
QE hae eda ales Be Gly SR dO Rte Oc ee Oe eRe RREN RD Chee Y ae ieee eRe ne Rey fre 89, 94 
BYE aANS Ope eR PON el eI on 58 teh Ake cohae 8S Ve Woe ee the stir hai alana + ogectgatlans 159.312 
OPTRA Laval 6 GOS Aig SEE CORSON RT eo eee a 158, 309, 424, 425, 436 
OYA oj ape Ml oe UG 2 eee ee a Sr 318, 319 
as arti 2 Oe i coca iss si sald os add. caskeuenasteN inlA ves «ee a euaveovomaaels 318, 319 
"Registry of Tumors in Lower Animals"... ......-. 60.0. s eee e cece ete e eee et ene ene eee eee ees 299 
regulation/regulatory (see also registration, permits) ........... 0... sees eee eee eee cence eee 264, 268 
STROSS. Se iB, DIRS arr een 49, 64, 292 
DTIC AN COIL OL gracias ger ih oe aren wlayace oinin oie mya gov ede opel sheve oles was 49, 64, 75, 76, 134, 135 
Pe est O OP ICAMCONIUGL ry Sere Soci hooi aur ain ead sitio eee ak age Shot « oe Mb aa ae eth eee os 154 
of importation of biological control agents ............- eee eee eee e eee ees 46, 88, 91, 154, 155 


aT 


jurisdiction of recombinant DNA research ........-..-. see e cere eee eee eter eee eee es eeee 322 


Of Pesticides... .o ieee Lage cok ce ess Amite ely oy cee e ne ueyene e Whe es eivacea leila se ane 60 
of recombinant DNA technology 24.5 .40: 22.2.5 20 ene teen = eee neler sels cee en oe eee 322 
release(S).0.) oeuna- es wes 50, 52, 56-60, 73-76, 78-80, 85-87, 91, 94, 100-105, 107-111, 114, 115, 117, 119, 


120-125, 127-130, 133, 135, 146, 150, 153-156, 261, 395, 396, 401, 408, 410, 411, 
414, 416, 417, 419, 420, 422, 423, 434, 439-444, 446, 449, 453, 454, 465-467 


ACTA sole Seek a a cw me Behe larg een oe clmahw Bie Sites" oh cutvau Ee” ayy gRel fn cene aie anc ee ele to a me ee 62, 446 
AUGICNCATIVE 2 sic c's = ele © kets ohemtad ys ae oak es ecomea Mater agra 61, 62, 103, 105, 110, 111, 120, 400, 419, 434 
broadcast % sccasec Gocco eg SUS 5 cS Tea aee ple WB ace Ciphe) ake: Bre Maw 00 Siate teagan tea ee 446 
INOCUIATIVE = «hen cae kv tee Bue Asan, ole cats ce hee» eats Vote ce ean gee (ocean aan ete ee 9, 32,61, 277 
AHUNOSLIVE! “5 oo. «she are eel, tee ers cone Groene Gh 2 rane sae nea es 9, 30, 32, 65, 66, 105, 111, 417, 419, 423 
PASS ee ce ste Vem ARIS a ecbseis elie Be Ure ne OG cr cist colece Ee mates ee ee ee 54, 416, 446 
Of nematodes 4. ose cng cces sats cde Sead wears Goeele wie bails = eee, Rate sae esol Cees 294 
Of VITUS 865k cle fe Bad Meade 8 bed caw ee Duden (umm eroulo. nile © pasta aD eatin ope IOUS Letras ins gt an Za 
POMOGICs: ches ca crs 6 i ta Wits wos Hate oats Sechuie otek od eet ee On 30, 31, 61, 62, 64 
Of sterile insects ....0 ic osu abe od oe eo vd Ge eree Fis eo aye 6 ao papiethig gece lets ce Ge gee eo 288 
"Releases of Beneficial Organisms in the United States and Territories" (ROBO, database) ............. 155 
POPOTten CONE rc Hak clle case go se haps © eee oe ease Bales coctatel Sos ea wee SOUR ae ce 324, 414 
Research Work. Unit Description(s) (FS) c. cies cars ctece acre fai © ls Sonia ene rmte a ere at cee 407, 426 
residual control, see persistence 
residue(s) 
ANUDIOUCS IN HOMEY fF nee ass ccc ay) en cus aie tae ake = cokes 0% ye eae IRA eee tri one en 274 
| 2 ea crate a nis Care nels Stenlertd Ra MR Ke An Goer ee ie tc Aware ee EG dlcrc con ool = 292, 309 
PCSUICIOG es Re rr leas ature tates any oth 2 Sie. 6 SURRRNE ISS COR Go nots, stots Nae nas Once a ea en 235219 
5 ch teal ae tte ote ply ae pea RG, anny Be Aeon Gren PCE Sci Pula MEL AIM I nod ea oe no + 274 
resistance 
coat-protein mediated viral... =. cs. cette pak «ele wie ctaeis ose gisele oa os ee hig gees) ae 457 
CYOSSS 5 scare AS Sia hc ek am Sala arate reg Goede hs Oe Sram ty AR apes ey ete aren ne 324, 415 
host plant. nee 6 eet arene” Nt eon eee nee eee ene 28, 291, 316, 427, 451, 457, 458, 465 
WYOTOMYCIM sin ois, sas Sy ve cine © 0! ceo CMe nie ee reueer adi «amis! 6 ala ease erie Sekt aete ee ee 414 
Management 5 yea Se eis en ee gece es anes oid wegen a ve ole Walkers tore ots wie is ee alee 415 
tO: ANtIDIOLICS fe eee ae eye ake onan nearer e cians ean ee ee 300, 328, 414 
to bacteria’, Gee cae ete sweet ae 6 oe Oe CROTON RUE one © Odeo en pot te een ue ent rr 328 
£0 Bt eee arte te ae ree tee ee RE Ree ne den Retaie eee 70, 110, 147, 159, 292, 293, 415, 431 
CrylIlA Toxine. ries Senne erent ia sin ae te oe erate eae tie age Ginnie an 415 
to chemical pesticides 205%. sqntos eee otha es ie nok e dla Cohasset ae ea cree eer 23 
to Chalkbrood ae crs oa ae «seers Reta Seine ns err ei ee ra ae ee ae 159, 2752320 
to. fungicides ©. 2c 8 5 dee eh ea ee Onde tat wee e tees 615.5 ee mere hie ak ket ae eae en 94, 98, 99 
to heavy metals (in plants) <a; Sm soe sone soe eee as ee es ee ee Lee ce ee 458 
tO NerDicides ss os el heels Vek eka Hite Oat aes, Oa eee ee) Sorat oo Sa ROT INA ral ch oe 90 
TO'UNSECTICIGES ce s,s Seat oss seaa 6 oes anere ene a patie thd ene eee eat ee 60 
to. TYSOZYME 4.5.05. 5 eucas Staley pape 2 ete he ete Ne ag seecan ae ek ae a aa ciel 323 
to nematodes (by mosquitoes) h 1k hiscn: ea aarderciectee «eee © neil ee neni nie, oer 294 
to Parasites 6 LEGG aan c d+ hws od Oe aes SERS ME’ Soe ape Sle ceed Nee oe ee 324, 444 
LO PESEICHEES 3% sree ars ss woe is werent ORI er a nc nT eee eee eet 29, 94, 107, 279, 300, 324 
to plangpathogens *y2h ri 5 2s, es 5 ona > cope eh teen aad en a En Sea ene ee A ee ood 13, 14 
to. viral pathogens’ 0... ioe. Fara 2 cokers Rite symone wee an pre emia oe aie 2 ee ee PAN | 
résistant varieties of trees cg. sels eis es | Sine eae ciescec nt sar ae eevee Se tact Sant we ea 106 
restriction 
CNGONUCIEASES F.8ae r cik ae oe Meh cee OEE i re eh ese 280, 311 
CNUZ VINES oe the al apata (Gem. oo ob a i258 witb Vege Baha oa in ohone: Crary eet v REA aE nts ie a fete ie ae 313 
rhabdovirus-like particles) s' i sehes sts ages tee ytd oe mee a aie tice ate een cent 300 
Thizobacterta fc geo als eee tele save ace eon cta eaten Ginter ae coat eee rere ene? oe 90 
THIZOSPere sts aN odin aa cee ahetat ae Ce ene recs ate a eee eee oe oe 41, 93-96, 456, 460 
TIDOMA VIE Zico she clone CUR Dee ie os en ees. CTR een ED oie Tan ano a 307 


ribonucleic acid, see RNA 


578 


risk 


COTESIA egies, lie AS ABRs EER BEE cee ere ee 88, 89 
en ee abeCa ta Alar CUT OMA OILS Barter cute RUnineIs go cass wd als elie egw RE eee wee Sin eteaee Amt ae 436 
eee 11d c Sane re re LAL Rao ah alpine aid scl dys! fi viehd % Whaew Fo Go's ne ds een bad mE 98 
RNA (ribonucleic acid) 
Re er aT CCCG ICON NE mtn Pat Ne Olin e als. aie «9 4e «via G Me dow Ai 8 8s oa, 8-8 aia se mw hems 36, 456 
rodents 
HIT PIR ay hE OE MA Eee 2 bg glvqilnr a 41d psn oa “a, o isok Te bw duuale“alhece FV» 305, 306 
SS RAO MEER cal MOVE pees aide bm keene 8 pel AO rg ete er a re ea er ere ara eae ae 321 
TREES gon 0 os 0 hee Dehua on Rep ea gee aT Pee SR 305 
rots 
Gf ar rer ee ee PTE hy Gof s cies ueis = tae ois ee genie aed 4H Bled 116, 456-458 
DOWEL 30 PRR SEES Sil one BEE eee SS ee a reer 66, 93, 98, 99 
RO OL RE ER ie ee es 102, 104, 116, 117, 456-458 
PaNVaCEOUSICGecea ISG WCCUS TOW CLOD) pare oa as ne Go ois iscics yo oils coe ED OMe os 5 bene cing 29, 39 
Ne a | ee rear aA Unt See Ma SMe (otic iia P4spc a wise Sia bows 5 Kind wed hg ielace See ew SajeuP ee Lae s 273 
S 
SALe AL SESLAIS() DIOSAICLY Ju arise). ap cicvaene mietshtuwe a. + 153, 154, 158, 285, 298, 299, 309, 310, 318, 321, 330 
Siren Slit Pena wan Cn eee OI RT ee Crete NL Fe eas A MRCMND Srl>, Soule e a @ 8 Slaw ¢6h9 Gund 127, 414 
CACHE TL) RIE Ly CR EM ra asp REAR NIN Seiad Gate esi GON dds CAE es eked Rao, oebe Vhs 3 ba 285, 425 
CEE ee S00 OX ae ere wee ey TS aes i fd af oF bos ve dla 's Fa, 2\ glia ses» aiard SR as jal 
Give ast ar DIC OMICAL COMO) oii cent Pie wr rin 2005 tsa Vigoss AG ame ee os & AW halen 153, 154 
EGAN AIO DOTS Marr ta usiy nm ey rete ier pinot din oils W Rieiase ¢ Grae ANA! 9 a dull cep Sheva 300, 310 
CEE TE USCS EE ere tea aed UR ge Ped TEM e Bicc a cts. qe tp tein sue ge os Ge le 299, 309, 318, 424, 436 
SUITE) COSTS oy ge aS Ie at Reg 129, 403, 407, 419, 422, 447, 448, 451 
SS OL IRC Me MNS Penne eM trey REPO Mee eas tenis rch Oars cane Goals ae what MEO © west SRR g 3 Ag ice y adn Od Banus 129 
MEST A Sue tae aa “auth gE NTR LEGS es eS LG ER cia ad an Oe es gd ee re 129 
eas a Pe Mee a hire eI kia ee Scie ce ga tae Rao oh Raine « wis 0b 6 a8 Bow chs 4. ovo he 432 
Seay LE eon Pe VNC eS Sky deste aS see o xt ah en, scepg ince Grilps sia qld 4 3-5 vee ala as 41, 275, 464 
Meee CLL OMMICTOSCODV AO LVL) Giese ae ts ais vse ka iG) » Grnitte ware ease ask wnsigtae: ald wid ¢ 45'% Hes > Re 301 
Bem e AmSIMissiOn.e1ecirOM DNCTOSCOPY. (SLM) Oc irue cs os «Saye e due Boi Saes oe cdg eosin wale, «atonal ga 301 
eIeGee GE OUCAION SUDETIOLSeLvICe AWAIG 5 ai. ay sine o oole tele os 4 ww) ctdueis) 40's Wiade + some witli sin hin tates 436 
Scientific and Technological Cooperative Research Agreement on Natural Enemies of Gypsy 
Rhian Ceseaidene PCOples RCDUDIIC-O) GMINA) son gteg cn tiers q tisitee oe «deca maoe is «ies nae 420, 421 
SRse INS CATS SYS MCE eA aceite Pere toes Shen qusticdm ot Coed deel seco ao ave 146-149, 163-165 
Bete aT clisEE OIC) Sean Are eet PA A AAT Neel ak, mga Ee A -siialg Wie, ah Hie le 's,0 0 SS Vusgeyal ae 403, 462 
Bee Ome T alg a eTUOL AI UMGeL SoU Mesure le no Roath beg Nate asc. ky at sfx ats 5 pot 5 Ca +b Kn ate, a Caen 264 
Ba Ot Ee far eas AEs Nc hah ROA ts Seve fins ie gidyct six Ps at ty 26 @ aya 494 #9 6's) aiBae dake oe ope 318 
Bee Re eraN Che Atl eee areas Me Ue ens ane fA an eVGl Sie ola. aide sats) edits dis. 4i » viel a wm. eee elder 95 
Peete tS en ee Cee eT de ate Pinca Len eee tle aks iS fhe 1a s.gha eels We «ators Wide « Rien 455 
selection, see acetate selection, artificial selection, host/prey selection, and natural selection 
RTO CTEIIL TSM Sn ee ctr so PO ual een eo end Aba o hoe bea 31-33, 61, 65, 66, 400, 401, 403 
Fee mee eee ee ee eet eer serine stad ee ald sehd y= 49. 418 Glo ks 2 A prsre'o- a Se vp camel Gada ale 400 
So, WTS TRVEL. 2.2 Wop te 20 Lg gue ae It EE oe Can a ti ae 291,297 
TENE ECALGTUS) . . 08 boli aakl eet lan Ae RO a aRRe Mies Coober Croke ee eacarrarmert ce Cie ee ee 40 
et ALN) MeN ee eR Rice RNs eka oh, wv den, V Sin A GUN Wee 4 &, eo Bde ee EO 305, 326, 420 
SA oc ER OT tus SCS A MOSER 3c 8s, ge alin Beal vray ch ia oy vs altel & 4c 6 Sms sganlen ad aie legal, ways 278 
ert EE CC ae OM ne US ON see Sh ia fay ahs wis, « mye sees oS % vgblb Aus Buel Mer@ln hadi gos ah 409, 412 
La (Fie SSRTRRG a Qa Gudke ate ge WR eRe OR IEE eek eC Ea Ee eee 28, 29, 40, 102 
Bete ISCAS I0 sas ade Per eisai hs 0b Vuk a> aka, «. ih ye CS nsnld Wiel ows ein janes tate ulus ou Avees! jie’ 125 
SUCRE aOTACLICES COMMOM A is fete cine ceuis oF) ss hy eases ee woe 6 8 103, 105, 397, 406, 407, 447, 448 
small grains, see grains, small 
sodium 
SNUG! <5 gc KAA. So RS ete GION Tart er ee ion Onan nD ee eee Doge Pa 90 
ree NOT te Bree aS NO eine es ce nie ad PORE Armes le sale ssa es 6 318, 326 


57/9 


INSECE PESTS ® La. yccdee wees of vee wae ew tarde ie 9.4 Bed slo mom > Peters ie elt gee aes re ee 287, 316 
productivity: 5.92) HAI IIN Wee ada een ete alemagis sane f sph> alte © tse mnie rele a 462 
temperature: 0. 00. LIME Dien DERE gin tole ly Gree o BU reared tet nt he, Rana a cit ene eee 316, 459 
soybean cake acc cn ies cis AONE A oage be # Weoley letesml elim «lolly thei lanslitels: aie «MH SeMiete aN sue Miva cae 93 
specificity 
OEBE «gc Vie esas aedlesd o 5 bp Pew Gp AINE eae BLUES 2 Gp STR as PAE altar aap sane rat ee es ee 428 
HOSE Te Gore ses aw cate eat eeeneeit sean eal fad 73, 75, 80, 84-86,135, 153, 276, 279, 283, 286, 308 
sphingomyelin —< nays cee de deedmeme nnn Ud a bain yd eee Op Oo sowie a) «ace wielee eurea were ee 306 
SPIdEr(S) MM ak. ue wn pe ea eas eae a eRe eke cae adie aes eee 411-413, 434, 435, 446, 448, 450 
ar bGreal OR i ovcune.b heh Hed Use he Pe A lati BOL Cae ee 412, 434, 435, 448, 450 
MUNIN irae. bbe deme ety op ola le obese noe 6 em ae gn oe eee a sees oe 413, 448 
WEDS INNING orc cscuyers «oboe time of aublen tra’ ai avy ele o aye" line iiop atin chan eta 5 r/o lar ct its: gt sy Se a a 448 
STUITODIASIVIAS > sso caso < F  ¥ ce aonletcheeqr tree ehesehe! dhe eVats one. aie Sactocaiie ate wt eI eee oe 298, 303, 305, 306 
spiroplasinology <2. 6.5 vswu ves we eae cnne swmndons cs SA Doe ee 800s aetna 0) ene 2a 304 
spore 
coat proteins esas 2h DE RE PL IS PE ee ERS A ten cade ee ei «oe 36 
PONMINSON cs aae.. Saiod <ae oruee eae see tie eas RE 6 wees ae, ee ee 284, 326 
production. in Bt fermentation Systems cnc ge< esses es vale nds en Ome Pelee ee ee 34, 289, 290 
Vidbility(in' Bt) eters: eae oa. mee ge ona aia ns 8 ta) Gericom leone ie ee 429, 450 
SDOFICIGES. fyic a cw osm Sele atere elie snes ASEM ea We ete GEL 6 ae Ate ir aierate 0 ee) 326 
Sporiilatiotivwy eyo ge doc aw He are ath eee oes 287, 290, 292, 293, 315, 322, 325, 326, 456, 457 
Stippression Of 5 wet. tee de oe ye oh ose Soy G99 eng. © ee sgl Pic eae eee ele 457 
Sprayideposition Ov iege ep arneias sou) Bee oye | SSM emn scien diea a, dt curs @uplmrern Oe «akties «(oie weet ee ea 431 
SCUMTOIS ©. ae Sette eccare Sepa 6 nataues RRR v8 dre Md Re 6 oie EAE ar op as elite PERE TS da) Ake 444, 448 
SUAPVAGION oslo eco rscrs oie OES ao eee artes Ot ea oN OR eRe eee Tee EDR ROE Saeco Tet an 433 
Sstenmdiseases (seecalsocankers) (O°. aay <a Selec see eae ence tered ees, Be ee 456, 457 
sterile insect techniques? cui. sts arene wee Se Heo Sheen ne ee ea ieee oe eee 25, 29, 288 
Sterol Wee oe. & a she eo wz ale aetis essa © adr We aio) fe Oe Badia ans dorct ope ca RR RS ten a 301 
SLICKER PE A iar). ov 3 gal a eeieaee DE VL wempe Gee OT Soe Oh A oes OP tegen 429, 430 
storage 
of entomopathogenic nematodess 1) fa ey hc eae we ee en es ae 278 
stabilityvof pathogenss vi... ccna cue care wonton hicks acne a kt SA i ants ot ee 310, 322, 437 
SLOrEd PrOMUCISi. eh. cu ater: omnis errs arr eee 23, 31, 36,63, 64,70, 117, 139. 276, 279ea 
STTEDTOMMY CHD Erte MORAG we. oc ig also & Mee i cra ch, Be ease eas ELON e Gan Recetea 004 is ee Oa ee ent 322525 
SIFESSOLS I ree erties oo figs hae ere wpe eicaga dike ans Ob lait ale Aon RRR Gate) anal oe aa gene eer 159 
Subcortical:Habitat’ * 0.355 Wile haa ee es are ee ato ee ae ee ae ee ee 408 
Suiblethal effects Pleven nan oy ot rk eae ete eke alae seca ac eR ne eee 272, 319, 326, 452 
sublittershabitats Wee cog Sone oa. co Wexies ice whee ee oi am late Ge coe aie tre ene ete etre 448 
SUCCESSION IM erin a AA 3.0 eu whee Rew eee CSN a ONE a) BIGELOW HEE OTS SNE ORG er Taian aT 461 
SUCTOSERIE GT MWten a se hw 2 bie se tates 2 tye ee emo ee Ed ok om aestebe cuneate race ete ee 323 
sunlighbinactivation OLMmicroOblal PCSUCIGCS, me ara metres srs sean eee ne 36, 41, 158, 290, 309 
SUTISCreelis/SUDITONE provectantsiers... sisi ne ate aren Geeta ae Ween keener pees 290, 302, 304, 307, 425 
lignosulfonate (aT £2 fats a pated £4 Oe ape dee MRR aber sate ree Ge ie oe eee 425 
SUrVey(S) Mens sn pare ete an ye ba ae 404-407, 416, 417, 420, 422, 433, 434, 438, 444, 449, 454, 460 
susceptibility 
tO BUR Re ae ea rene eee rea Mer tite Ae se Rae ee 429-432, 452 
sustainablévagricnltremae Me fees cad oe Woe ee Seen gen ahine a tee eke eee Rane ee ne 133, 136, 285 
SvimibIOSiS/SYMbIOtIC relationships. ....25... eae eee ean een 276, 285, 286, 306, 414, 457-460 
SYNErPISNI AUER aa OGG Reeds tad te RaS eee ae ad eae ese © oe weer ee eae eer 159, 430, 432 


synthetic diet, see artificial diet 
systematics, see taxonomy 


T 


"take-all decline" (see also Taxonomic Index, take all of wheat) ........... 0.0.0... ccc cece eee eee 22595 
tank mix 


580 


ee EER GP MPR MER ORB Oe Fl tae et Pere Ym a a So eS heels Roetinsbeon as Geaeed poke ns. Haan avenge belch one OO ANOS & Gara 314 
RSC a Ne MO a Be A les ks a aduitins bred. hs iis eR aivtieonsaes seid dol Maswniwedheallewkoavs 24,44. 45.48.51, 148: 150 
Ss MCRL AN COU SE ATII SEU Gene Me RTM BND SE Be atic WAS Bod. erecta peas wemcat ke oe oPonnwybueodyeeiri, x: ARMM AECRNES 6 Suleisl A 150 
ALE a RN ee Mo hs oe eC, ci PeR he «sca eon dhcas ec ielg SAE ERR ee iran thas es Peas hike 45, 448, 449 
ERC eA aa AUG SARE PC Ae AE a Me dt fe Cn ee yh ch Ducato e a shakes ob canis canyon nara niin: tesaiva thes nn Bi aed 130 
PUES 21 Cat WRN RSP gw cg 0 icp es ah AAs Sigs pels naSMb vk pSidgu drink smsiivecaie, aN onSjlags CMAs 130 
OTN ONCE CCT) ere ew ee We AMPA EE wo WOE Si Clirds Ad thr -nthontwsud ica deooniltr nahi ecennttonncPensssweotagee slaves 48 461 
SILC CCL E Me ea eed Oe oe oe ed, PPM Sr EOE OR Rican sncstcaihewib eR Ph oe eats wc" touas HG ck Ped temas BH 33, 40, 68, 92, 148, 286 
POOL AL ere te ee ney Mel re NER, Lov Woe he sup Mecsinray aa ar sdoatdanepievons Pak dw acy APC 35, 276, 281, 284 
Le on Bek es 5 ne RG Oi Oe Oe cs Gate enh oe ee nee en: eae eee a ee a 148 
technical grade preparation 
A! UNL) oo Sse) coy 2a Ea cis) “ruc, A ages ne Eee ek MORE ee a 436 
BRC ILO ET NGL Mien MR PS BMY yy cae the ee even c Cain Ten rhea ovanay Sad Dac a's Lives youn RN Melee Pe als 92,94 
Be AG OeIC BIG LIC (6 Wr ee cat E cit WTNH top cto, eR yo enrey Sas anor nachtnck dase eg? CPE or hd ao 8 SER 3199322 
Mer Arey Cul) OXY LEM AC VCLING MY CLOCIOLIGE shes sac nie eee shop sctads oben oie) onal rotvontnes were lice swtpeinel dy, Sue 2745329 
PESCAC ECSU SAD LEZ) DOCS Meee MRE SEA chal trncMee bona nde cicada Siar aig te elles wr dial-sb ay mE ONS ZOE OS ye eA a 
EROTIC CCDOL cater eat WW BW a ae RR ieee n Mtoe eso tie araitete Aetna guahan aor ice) gal xurhl's: EULA 1313132) 142 
SEES INE) ELS aOR er ka ree er eta arses leg oe dO NAME cy ce ys! sone rotcvh oP deste RAMMED vidas on at'ahte cop aloe de eporse MU eG 413, 463 
SPEC 1 ame ee Re, Ane eS ota Pe Se ota cd ot a ARM as avo ade cww « MOEN 430, 451 
SA VemILe crs A eOImisOrsa WITUCL) wagea sia Aare ee oy aiden chew Gat goa aiaeue wand n Hg w hates ae 442, 465 
ISSUE CLE LIPOM SEE a ISOICe ACHILLE Jim meres cre oasis Fo 4 rosacea hats Sielat whees lotwewre weelbhe « By TO I28R303 5311 
TM, see Terramycin 
tolerance 
COE RC EEY Bree A ty Nobis Shu ital est aap taenen MRA aah ans 2 A BRE oN GER Phoebe 458 
NEEM oo. seg ae, chuntgy AE eS Oe ee <5 460 
HINSOE Ee em IMEI SCCLS ) eee Wen ea eae re en ee RO ME gy Noose a ha aS Nghe gen: Sys wea “atotaye 4cd-a cots 62 
Pees Ma Tae Pa ereRL MG Sess ova ATs: Wie sleyid Oe a SPA ph al als chin A wd nw wihtke MAM, RRA ERS ALP dee 454 
Voll ocr mre ee eR ele ee eC Cine esa ads Une le OE eel kote ek dame k ee 2 307 
tolerances (regulatory) 
ee a ghee rst eG AN co mew table hon biden vor ein dea 0-5, ANAS tals STEN Eg te 287, 299 
PREAH omMeMALOUES ALM ae exe y shed shape etal lotsa es rv aivaeG wemig, a abe ate ae dsais MA Aaa 69 
Fy A eR ARR deren eed Pips ter ts ah ig adler WINE aha, AP gg Rs a Ie eg PEAR pe wad ah te 319 
Pe A a ee ER ON Tae TO ER Ae Sid ci nln. s See TE Te heats Mae oa Da HE RTA ees 35.159 
NC EE eRe i Re ci eg Monat es Ses thes oun ee a Pine Oe CE as eee, SEE Tua 436 
SYEAES LMP ry Re eT A, ie er tan bre apg ahd 9 dow ards Giada SL OG GO, 159, 430, 432, 451 
LSE me SAP NS es Pek conn fas desc ychcins neha Pt raes eon tca- VE bd Ed aca SRE, FO MR SEAL Ma 113, 436 
ra bov jae PAPEU EG ee ae a ee lc ote 5 ace Sg ee ete re en en 113, 321, 436 
CIS CSE Pn TE eee eee pce ee ENN AT tisha se oiarbte aia tab ei eae hiokios cauavareeuid box Ryn ete 435, 436 
transgenic (see also genetic engineering) 
SAE ERLE COPS OCIS MPMI x SV ha ca laen ss ucratr Newser alte efor bs aden tewunhs ates de Sora Mawnirsand.whiaitatay wanngal dae ene oie ann RON 135 
BN CULS) 220s ae Se eee ee eee ee en. re 292, 415, 451 
PEAUGO VAC AMNIOTIC ATECE wae Ea a haytt/. do i heehee A sdacw ede Wen ottn Gee. he china Ol Soke Bik Gul Saw « 276, 305, 415) 452 
transmission 
DIONE Dee PAnOLeNS ac. rennin Si ee LANL GAG ARR See e wane VASES a eee es 298 
AETV IEAEE) 5 5 ek oe 0 eR Ns et eer ne ee ee ee ee 283 
CHIME OsDOMtGlia wi -wregr ont obhk nthe eiiEk SAxialok SA wile SSMS Ane ipo on ace SIO CE Re ed WV 313 
SE Oakville AtDOCENS Renin cei cas. 1c BOR Ne WS Shs oma iniG ak has SAMO Rae he ss 457 
CUE OCOZOR See Pre Cea hear paired SS eseeml hn A anda IacaTiaties ahioms VarniaKinayn ADMINS ND aM 35, 276, 328 
CETUS CS Ee a i phe ah bese hone hye resi maaan ga wegen Metered Act. BA ALIN 35, 281-283, 288, 289, 319 
OL viruses by parasites/parasitoids/predators: 2.64 cara n ee nae bs tne vue ee 103, 111, 271, 309, 419 
ERIS LAPIS MR EA poms aise eet Pa on Sn aed ho eMC WRI ian Aaa Meg Su See BAO Po 400, 402, 449 
REE 8 Sn og) dood Sia A 2A Gen ibe oc Getic Hn ae kc a ee ar 423 
(nal dise eee er een re ee: ee Laem ee, See SMe ree lisa ds 448 
RINE ROHUQ) DS: yecng ae) c ich Ge tn 9 Re ekchonnee ihe 20k ae pee eae 402, 449 
DIA ee Re Leni Nien ohn HOLA STAGE EUSA LARUE LARC Ree eae 448, 449 
ey SMES “yoy ay EE ee nr a 449 


581 


free nuts 20002) dh Be ee ee ee A ie ee UR Ae ee ee eee 276 


TFEE-CTOP- ECOSYSTEMS. fc eh tere lbiy cee teks eceuvacs lee 2 iris ne leur el eels narra Gaerne ee 412, 413 
tree-tiir ecosystems: Mey Weak cians Weare! ek ltle adele Sanya, 6s 9 $e ter taseniekess ts el mance are eee 412, 413 
tri-trophic. interactions... 4/<.qii< smtereho sibecltewe cbr + pice seisheteds Gua leases oprah eee ae 427 
triploidy, mechanically produced for sterilization, 4. 0. 0.0 e ya wots oa se Selene Free cleo iene 128 
tropheallaxis sec lepeiete. spas Shenae Wat's orbs Da eee epeuspoue tens se V)s sill cntigen as gua tp eRe det clo ay it antl Mem eee a at ee 213 
TUCK CROPS. Hs: bs siete oncanrace: hive beets ERTS epi Sone Eek nan Res alike oles ok ick ot ee kc ea 310 
frUP Aes ao cig os dhs, « ons phasors s: cooks aie hates gieue ele Paw eneca eich achicha) =. Sees ede pty tape ar 458, 461, 462 
fimo RECTOSIS factor E50. acer wists seen wiv iavsl fotos aie ninanoescdpariahcsey cums eee tae: Teena eee 305 
TRE CUT ESTAS "BN kes saak Guat WG ele Pett eee toate bs ap sep eee reg eases ha ce ee 27, 299, 316, 412, 413 
Tylosindactate o.o5-<.than'sec ns, uisnsishotiotensioty. Soapei caskets qucias.a/trokei stays tehaeenthinlisor ook hy mene eras ee 34, 328 
U 
UDP. (uridine diphosphate) 3 j...4.0i.0 sistas ss ted wath op adn eens bovbes) Selo rsliel «ae Shs etoges ee 426 
tiltra-low-volume (ULV) application’ «..c.c'asccawiafeas, + «5 sie beat aisle th amtin wo s+) 2) phere ogee 451 
ADIT ASERTICHUT SS es 5 Gives av Sieg a: aod cise Sh slo is aot alow sl v-sv woot 61 pologloncon Re SRO aR PT ee nee te a 92, 276 
of Bt:GryNTA toxin damage. . ea.s wise see sita the Spin) = om ob a ae ain es eee ot nena coe eee eke ee 415 
OfMICLOSPOLICIA see ho ay when eae ao sete oleae x ssh alee role IR eed es ete eel ane ee 276, 284 
Of MEMaAtOdeS Ne vee senctaet ites hes iia dee. he baa) ates» She aS Ane eel e hea ae ee 92 
OL PrOlOZOa Mei iiss is ac gils ae, ested wheseres bs alles, aatyy eh aieee BUD pean ele, ogre «mae eee ee 35, 276 
OL VIFUSES, << os. 2 stewed osc aS One 4 dis okay a latin Cape aoa Seg uk a ie eee eee ae 276 
ultraviolet light, see UV light 
WNELSCOTV ae pak nt hes fae fae ig cua aire leg WE © Be maha BAS Buen ee enuesmegt aie ere 46] 
UNE Ven- age Stands saeco 5 ee en oer ne ws tole Gertie ins) ile a anenn Gre nate ah ee 447 
universities (see also specific universities in organizational index) ............ 396, 402, 403, 410, 418, 428, 
431, 436, 439, 444, 462 
urban 
areas, classical biological control ints cova. sora setae ven oscar fist tie ae 157 
POSES oS Pc gions, & Beg Hass eyater AO a stone « Sete eats aucge a's dicey ic Ae Vata crue gate sri so MONA anette ane 331 
LT IG ACI Gre eh = gia as i i Sees eS om See BEN Resmi e/et tee Scone ten earn nr 307 
LES 2Bivlogical Control Act, proposed i207 5 ae sane 2 eres bauer ied ae Gee te 154 
US..Patent(s), issuance ofc. susie, +x % culls ea se ee ee ce be ee 304, 323, 427 
U.S/US.S.Rascience and. lechnology, Agreement a... 7) uu. ee cles fae ee ei 420 
REV alight ets cas Jor at? ae arctegte ee, Aenea mene a eet ee 71, 99, 158, 283, 290, 304, 307, 309, 319, 327 
effecton baculoviruses a5) As. a pe neg ree toes ore oe Gee Cree tig ors aa he ee 36 
protectants'(see/also:sunscreens) v7 ete neh ne ain oie eee ee ee ee 36, 290, 304, 307, 309 
Screens, (seevalso sunscreens) ) 3, 3.5 an amiertutictc Guns ccncuchets Se traeaoilin cies merce cee a 430 
V 
VACCINES 65 jb se die eb didraco av de Sd imei ee pete ee Spang, hel oa ap ia ieee» ea ane: Di awl oz 
variation 
PCOLYPIC As ledaniersieas earch Bic uncnd sMpaiwe ele Fe, ghia <2 oa vhee sacs ole w 9 Sra orameieace vga: ok we en oe 462 
vector(s) 
baculovirus.expression: sry < select ar dercuy nti cit ee heeier cara kee Seah eat rel froin oat 302 
CIONING Bie sy gisie ver g We ews pine bay wip ee SOP ORE eres Roe EE ak Os cen, | a a en 322, 324 
Of bactetia rs ecu Soy ce Bh Bees re ae en eee een ead cela Alton a rece eee 33 
of bluestain fungus | 5.52% 25°) soy wee « pou Ae y oe ated Us deine 2 oe 408 
of Dutch elm disease). <5 5 desde coy gece nes ede Gene ow ee ot. le ns no ee ee 401 
of endoparasitic fungiiereisc. 210g ee os oe tees 6 atl whas bees to ee ee 287 
of insect pathogens by parasites and predators ............ 0.00. c cece eee ee eecceeees 271, 287, 309 
Of malaria yy) Akhter oi see's on ely daly x ohete teas ed ik ee rea ait sae 70, 284, 294 
o£ mycoplasma-like organisms (MLOSs); 32.4 22504 soe os ee ee ee 306 
vecetables vegetable ClODS aan ae ee 29; 31,40, 94, 98,.99..125, 267, 270, 281; 282 534g 327 


veterinary entomology, see medical and veterinary entomology 
viral occlusions (VOs) 


re eee ce SRT ee en eae ee 301 
WIRLONSS, sca, stcniehue ao nsec epee wig tae eed ve atte CREE de nn eee 70, 282, 283, 300, 303, 311, 427 
enyelopment Of .i2 9.06. sag 0 Ste e.a eka oc eee in yar a ee eer 283 


582 


CONULERE RY oo seni dap 62 Poth yOu © OSA] EELS Poe RU geo Ene ee ae en oe ore 310 


Es ods mw eCPM PS VGC GER eed EN REN) a Sorc)! icdaavonsnareh Wel adnan Slogan dr aa’s SEONG ve Teele. 301 
virulence 
ELESEDE  ectibence sat) egg Wedeetelo Oo anh eacans CCR ier ora ean a eo a A 318 
SS La IEE Se WL Rtas BNOP IP ae Re A ALR Sygate Suan oh atsbote ghey dhet angina atlgneh Shal sarlaian ae) 2 296, 297, 308, 311, 456 
APLC AT ICS at meen at Pete Nan? Wu tte A MPnereh ven sshardest chord cee wa iy gsherwehane arate oo oh SOLE 312 
TE TOR ager Gate a ERD OM Mag! SEA geiko Sia RE ee ee 312 
CEnIe NAO CS mE te reer RR ah nate cee eects Bi ndeestio £409.40 4 din Aid «i, Pale oribate wow Co 279 
CTECATUSES rt eis here ate sean ea Nae cease ye eae cs 280, 288, 291, 301, 302, 304, 307, 308, 311, 318, 425 
MATUSCeS | eSeer VITUS IN taxONomic Index alSO) "a0... ede se hs ce yates 31, 35, 36, 69-72, 98, 414, 419, 424-426, 
429, 432, 433, 435-438, 451, 452, 456, 458 
RUE GUS SDLAVc Cree meer rT aimee Ne irre ee ink nels mice Gleyutis es e/a dun a een aidiaye Sims 4s 283 
EMmOmMOCenous ENtOMIOPatnOPenIc of yens. 22. 6s sense scene ane 158, 270,271, 277, 279, 281, 294, 309 
SRAPACERIIAIN EC VS) ee EE Noe ate eg wf is oo lal ald uscd ceed we owe! Re yew fs 3 301, 302, 310 
PSEC ACTIONS Mee NT RY eee Fee SNP R ae oot Me eae eed Ob kp eb ae’ 279, 302 
POSPSIISCEDUDUILY (OM mnie tren ite tc Gaunt ne. ane etemics’< wet ye Gale sare ees ¢ 280, 304, 307, 319 
ASCUUES EL Yen ECAC UI OCOUICLIOL) IEEE eae ste ne Or em a feline ut Rem aradky by cvs: Cotte de ca ws we os 280 
PASOC OT Pee ee RR nL crates ate erie wi ee Qe 31, 34-36, 103, 113, 158, 159 
Bee ALI CICS aay MESES eT ete ee tee a a Pre cet tience ek | ERM Ec bas & bray 2 5 de “6 ad 281, 300, 456 
myco-, see mycoviruses 
nuclear polyhedrosis (NPV) 
Pypes mr Memmi e CADSIOS) Man nts oni et a ee ates ccs ee ake cut citer Scie. ¢ SI 35.00 
RC ACME MP aM Ee Renee rte ee ors Pee cy tne s gate aims aki eS dine E3\ 270, 277, 280, 301-303, 426 
RNA, see RNA viruses 
Sta ity) aren ee eee RNG een eS Ee oe Cu Ree 277, 292, 304, 307,427, 437 
Petia mMIOICK OLE Tey ere te. ee Ue a See cots os cis ROE no vee eee eye des fs 202 o 
CETUS SAVIO 2 os. ochhuatthguentn cacieema Jo daar tee td OM aa a a Ne 302 
WwW 
wasps 
Mara ectill eee eee Rare a ee ee ee Wier s ie ey he Ne uae Saws hs wee «a 446, 448 
elie TPETA EES on ce celina ye eter thie lies clone fA a PW a Se Re Nie SA a 260 
Weed(S) ce chs. 12, 18, 21, 23-26, 36-39, 45, 47, 49-52, 54-58, 73-91, 96, 100, 105, 120, 121, 123-125, 128, 
140, 145-151, 153-156, 161-165, 260, 261, 264 
SUUAUICMPES MON eu eee he ae Ch ease ety wa 38, 39, 56, 57, 77-81, 84, 86, 128, 149, 154 
Cr CrOUs | @apoalales: Diassicacede) wan onty elect cn pues Cty + ote Ge pel te ke es nN oes 37 
ECaIOIICHOSS UG [Om anne a ee er eran ne Ms kone es Char cee an Pele Ey tuk ce ty le is 75 
CEC nae Pe ee ere re sre yh Ch or tire wen settlore dt aol ea ale lace ela we gale ds 105, 108, 156 
LLCS RTE Ce ed rier ere oy eeu hie NOAS teats Ripiere wie oa Yale Beane 104, 119, 466, 467 
AIAG CCAVIOUI orem CE tet ete Hit <a diester etal eae aiante. iar ay drivers os otal a ehalgia felniriialie sale ete: 2 Se Seaew WU we a ee 261 
Le ee Ee tO ec MEN Ce oar Rs tah nut brat aahe eG WWE wWla's Oia wee 4 81, 82, 86 
ERIS. cad o's albectondit he dior RG Bi dance Ua thas euch eect hla aene ery ee ane ea 37-39, 77, 81, 83 
MAN SE LATIO MPN fm pci sf yoi 2 Ui site tis.e ares fesda 21, 37-39, 74, 75, 77-79, 81, 83-85, 87, 90, 121, 124, 162 
TS ORCL ON) MteaM EMC a eal Nevins Wa sioils a) tg eS Beis h cae ers saa Shaye els! Viale wig (aunt's is, SS bias ee we sree « SOFT Ol, OF 
Cy YE TET og gore ence Bao 2 coe hy RSI PR OPC SOO el OR Is 80 
Se TEES. poe cc aoc Puen Betta, caer Cie eo ORE RCE MON oC OEe ae na iar 56, 77, 83, 154, 162 
Ren Pel Ce Se Te eee I hate atric) wie see neat a ales ioe 4/E tage ae saws eas 405 
wheat 
ee ee ire Gans aue sie Mee be tiv twee ears Whetiars 94, 291, 313 
CIE. coy AS ee yo 1 AOR AAD OD OA CIC nei: EID aC Sener cor Sty caer ecient i ea 90,91 
STEERS OIE. ean carene <ogieirad) opiteahcihl aa PORES) AIRS ee AR aR nie eee et a 293 
Dritclerrecstirencte ernie erent ak nds dad alvecule N's odwav awa vaceeeees 405 
wilt(s) 
disease of gypsy moth (see also NPV, gypsy moth in taxonomic index) ............. 0. eee eee eens 424 
WS ALTIENS oo. ea Pvs tee silion Sasori, UREA EOLA AO OR ee ae ana ar aa 118, 457, 458 
rad atl ee a a sds connie base yor see hele ewe ME HF Rea OOK he G86 412, 427 
EE ict MI re, Fah ce aut ils SRE GAYA G'S: ahah Wap lane ae HM ae SE BIT es Ce a wae 308 


583 


WOOD ECAY «sions spac ven wis meoneyere lib lyr Sie aeahanactees “as birde(#emoueytser=: see anasto taeet Relea eae 105; 107.083 


wood preservation technology. ..:ods cee. tle sic s0'e1 sais # ncn le meine iennasls erated a 463 
Wood products Hagia « p.<afclan nonce die niyerns spe ete tag rie eielake eds ie Geese tere ae 463 
woodpeckers ais aials. «oc ceusin ed ghnsanaloaheyaedes tient, 00 Sy nlnaled taco e cs Maree nae a a 396-400, 450, 464 
worker health iste s fold scscekks Genes Yale Ke RCI CUA os ln ino mp cn Se) «le Ye wages ace Sea a 424 
World War ll csc cnc d oa che 4 ame dn cuhlae sate Suede aye yee ee uene mie ebb, oy nyheter ee ae 297 
X 

Xeray(s) A: Wa BS. OR A SR oe Soren 411 
Xho LE DNA: fragment. ¢ 4.6 5.600 28 oe ewe 2 haps Jo af ie ae eee 311 
xylem ene ss POP. E AR LEGG, RARE certs tes oles ah oa eke ee 119 
yi 

yeastS::. fhe esos sen ence dee he lee ea he ve Sahai Sele a nanan On ions U e 99 
yield oe. ee ee ee ed seo gah Oeialbi ns See es ae ake Ga oe eee oie 121 «124,029 


584 


TAXONOMIC INDEX 
Compiled by S. M. Braxton 


The text contains limited taxonomic information about the species discussed. Authors and higher taxonomic 
affiliations were omitted, in the interest of saving space, and in many cases only common names of species were 
used. This index cross-references common names used in the text with current scientific names including 
authors, and higher taxonomic affiliations. Frequently published synonymies and alternate common names are 
also included. For insect species, we have followed various catalogs, with common names (where applicable) 
taken from Stoetzel et al. (1989). Insect common names not approved by the Entomological Society of America, 
but which are in use by USDA researchers appear in the text in quotation marks. The index includes order and 
family affiliations for insect species. For nematodes, we have followed the higher classification given in Poinar 
(1979). Class, order and family affiliations are given for nematode species. For protozoans we have followed 
Hutner (1978) and Burges and Hussey (1971). For bacteria, we have followed Skerman et al. (1980). 
Classification of bacteria above the generic level is de-emphasized in the above publication; however, we 
provide order and family affiliations where available. For invertebrate viruses we have followed Adams and 
Bonami (1991). Classification of these viruses above the family level is descriptive, based on viral structure 
(enveloped/non-enveloped) and mode of replication (RNA/DNA). These descriptors are provided along with 
family designations for invertebrate viruses. For fungi we have followed Farr et al. (1989) (for fungi on plants), 
and Humber (1992) (for entomopathogenic fungi). For many groups of fungi, order and family groups are not 
broadly accepted. We provide class affiliations, and orders where available. For plant species, we have 
followed Patterson et al. (1989), Terrell et al. (1986), the Germplasm Information Resources Network (GRIN) 
Plant Taxonomy database, and the Cronquist system of classification of the Angiosperms (as presented in Jones 
and Luchsinger [1976]). Order and family affiliations are given for plant species. Weed common names are 
taken from Patterson, et al. (1989); those common names not approved by the Weed Science Society of America 
are listed in quotation marks. Common names of beneficial (crop/commodity) plants are taken from the 
Germplasm Information Resources Network plant taxonomy database. For all groups, any disputes concerning 
validity of names, classifications, etc., have been settled using the appropriate ARS systematists as the final 
authority. For this assistance we gratefully acknowledge the contributions of the ARS Systematic Botany and 
Mycology Laboratory, the Systematic Entomology Laboratory and other ARS scientists, especially R.A. 
Humber, J.R. Adams, D.A. Knox, C.L. Wilson, K.J. Hackett, and J.J. Becnel. 


A 
Abgrallaspis ithacae (Ferris) (Homoptera: Diaspididae), see hemlock scale 
Abies (Pinales: Pinaceae) 
alba, see silver fir 
amabilis Douglas ex James Forbes, see Pacific silver fir 
balsamea (L.) Miller, see balsam fir 
fraseri (Pursh) Poiret, see Fraser fir 
grandis (Douglas ex D. Don) Lindley, see grand fir 
lasiocarpa (Hook.) Nutt., see subalpine fir 
spp., see fir 
Abutilon theophrasti Medicus (Malvales: Malvaceae), see velvetleaf 
Acarapis ({Subclass Acari] Acariformes: Tarsonemidae) 


woodi (Rennie), see honey bee mite 
Acer (Sapindales: Aceraceae) 

rubrum L., see red maple 

spp., see maples 


585 


Aceria ({Subclass Acari] Acariformes: Eriophyidae) 


nialherbe NuZzach? 2 x VEE esd whereas a wR WE ha tee wei den ea een I oe 83 
céntaureae (Nalepa) ios cin ie sees one we ye ace ies vb aren arn, olde Re ellie olan meg th 141 
Acheta domesticus (Linnaeus) (Orthoptera: Gryllidae), see house cricket 
Acholeplasmnataceae [Class Mollicutes} 25.909 5c. ccc sy Sa red eso ee et cles nel ae eee ee 305 


Acleris (Lepidoptera: Tortricidae) 
gloverana Walsingham, see western blackheaded budworm 
varaina (Fernald), see "blackheaded budworm" 
Acremonium breve (Sukap. & Thirum.) Gams [Class Hyphomycetes] ........... 00... c eee eee eee 98 
acridid/Acrididae (Orthoptera), see grasshoppers 
Acrobasis nuxvorella Neunzig (Lepidoptera: Pyralidae), see pecan nut casebearer 
Acroptilon repens (L.) DC. (Asterales: Asteraceae), see knapweed, Russian 
Acyrthosiphon pisum (Harris) (Homoptera: Aphididae), see pea aphid 
Adalia (Coleoptera: Coccinellidae) 


luteopicta Mulsant "5.0.2 saes cs hoger ok OSE Re ny pee, ohne eae a ore thre ae Gere © chan ee ct 339 
feiraspilota (OPC) eal) setahe enc eaten Oe ate elec eye eetene ae ee hace ate ee 538, 339 
Adelges piceae (Ratzeburg) (Homoptera: Adelgidae), see balsam woolly adelgid 
Adeigidae/adeloid (Homopteta) ico taetan ung artes cya. coe asi een ane ene ae 453, 454 
Adelphocoris lineolatus (Goeze) (Heteroptera: Miridae), see alfalfa plant bug 
Adonid variegaia Goeze (Coleoptera s COCCINCIICAC) a an rote erick rc cea 538 


Aedes (Diptera: Culicidae) 
aegypti (Linnaeus), see yellowfever mosquito 
Sier7ensts (LUCIOW) ea a aie horas GiOe BOTs ae ye bee aes Om et eu hcat ns cae eee ree i een een 281 
Aegilops cylindrica Host (Cyperales: Poaceae), see jointed goatgrass 
Aeschynomene virginica (L.) B.S.P. (Fabales: Fabaceae), see northern jointvetch 
AFB, see American foulbrood 


African Tues Peganum NOrmala: ee sce tee oe tas ct oe ee oe a ee 82 
Agamermis decaudata Cobb, Steiner & Christie 1923 ([Class Adenophorea] Enoplida: Mermithidae) ...... 1] 
Agapeta zoegana Linnaeus (Lepidoptera: Cochylidae) wa. .e  t ee et cee ee 85, 141 
Agathis (Hymenoptera: Braconidae) 

pumila (Ratzepurg). © cc tiac. can ice ache ite ete ee ee, Re ee ee 15, 114, 440-443 


pumilis, see Agathis pumila 
Agrobacterium ([Class Bacteria, Gram-negative aerobic rods & cocci] Rhizobiaceae) 
radiobacter (Beyerinck’ & van Delden (O02) KS4 era ee eee ee, 95 
tumefaciens (Smith & Townsend 1907), see crown gall 
Agromyza frontella (Rondani) (Diptera: Agromyzidae), see alfalfa blotch leafminer 
Agromyzidae (Diptera), see flies, leafminer 
Agrotis orthogonia Morrison (Lepidoptera: Noctuidae), see pale western cutworm 
Alabama argillacea (Hiibner) (Lepidoptera: Noctuidae), see cotton leafworm 
Aleiodes lymantriae (Watanabe) (Hymenoptera: Braconidae) ................... 00.0.0 eee 419, 420, 430 
Aleochara tristis Gravenhorst (Coleoptera: Staphylinidac).=. «2 janes neice ees ene 28, 58 
Aleurocanthus woglumi Ashby (Homoptera: Aleyrodidae), see citrus blackfly 
Aleyrodidae (Homoptera), see whiteflies 


alfalfa, Medicago sativa 327s. i558 «eet ee ee 27, 28, 42, 43, 58, 162, 314, 325, 326 
alfalfa 
blotch leaner; A oronyza jroniella |.) 4 ee ee ee 25, 42, 54, 56, 58, 145, 161 
caterpillar, Colias eurytheme, see nuclear polyhedrosis virus [NPV] of 
leafcutting bee, Megachile rotundata (see also chalkbrood).............. 34,70, 1241593324, 3252320 
leaf spot, Phoma medicaginis™ oc. ¢4caines os Vitae Chas Tee eee re Ce 98 
looper, Autographa californica (see also multiply-occluded nuclear polyhedrosis virus [MNPV], 
and nuclear polyhedrosis virus [NPV]).. +. 00 ee oe ee 36, 69-71, 270, 282, 291 


plant bug, Adelphocoris lineolatus 
seed chalcid, Bruchophagus roddi 
snout beetle, Otiorhynchus ligustici .. 0:14 usacu a sees See ee ee 24, 54 
weevil, Hypera postica (see also alfalfa weevil fungus) ...... 7, 8, 9, 15, 24-287 30, 31, 42,°43, 53. 54.56: 


58, 121-123, 127, 128, 138, 145, 146, 161, 308 
weevil fungus, Zoophthora phytonomi .., 7.4m. sg ea ee eee 308 


586 


BIKAMUDOE Hy ONITE IN ELANICEE ammeter ret, eile PO were es eT A el 34, 324, 328 


mrantenemaidae [alass Secementials: ylencuida)yies. + Hrs ake els ee er ONL oe ie 536 
alltgatorweed, Alternanthera phylloxeroides' 2. 60.040 sc Pb Te iia es ooh ON ON 38, 39, 78-81, 87, 146, 161 
Allorohogas pyralophagus Marsh (Hymenoptera: Braconidae) .............. 00 cece cece cece eens 128 
EAE SCL CIS Eee T eee ee oe eee ERTS ide kine wld Pada le be os EWE Sl One 276, 278 


almond moth, Cadra cautella (see also nuclear polyhedrosis virus [NPV]) ........... 30, 276, 279, 299, 300 
Aloysia gratissima (Gillies & Hook) Troncoso (Lamiales: Verbenaceae), see Texas whitebrush 
alpine 
fir, see subalpine fir 
Alsophila (Lepidoptera: Geometridae) 
pometaria (Harris), see fall cankerworm 
spp., see cankerworms 


Alternaria rot of blueberries, Aliernaria alternata and A. tenuissima’s 08. 7.008 oa a nc on os Pee. 99 
Alternaria ({Class Hyphomycetes] Moniliales) 
alternata (Fr.:Fr.) Keissl., see leaf spot of tobacco, and Alternaria rot of blueberries 
HOUSPatnOgeniCnso acs OL MMerre ern tan tse ie ey. Re Tn ee, WME. 2 ORS. AE 96, 97, 275 
EOSSIGC NV VIS Tair ts AN ee NNN Ht td OR nite a Pee a dna Lae AVS a Ooo 4 PR oe te Os 89 
CLASS SACC) IR ADUS MME eee eee tne ey) Sn eta: vo «| <i PORE ATLA ed OLD OPS a 89 
eiraniiy (tlalist.) LUbAKP Gc Nisnihara ss; meme ee ee neh i ee ek Ce OPPS 89 
SPpe meneame Cote ae cree rth siiiivicly vuskisies stoma AMMPna ees bone eta s ay eR! 88 
tenuis Nees, = A. alternata 
tenuissima (Kunze:Fr.) Wiltshire, see Alternaria rot of blueberries 
Alternanthera phylloxeroides (C. Martius) Griseb. (Caryophllales: Amaranthaceae), see alligatorweed 
Amathes c-nigrum, = Xestia c-nigrum, see "spotted cutworm" 
PAID OSPONE CINIICTOSPOLIGO i NClONANMCAe) fg m occle CO alana seo ee eo a BS 284, 295 
American 
CCSHTERU TCS CIS TTIC LCT CLO Me er Maes ee oh Se eg Dishes RRP Se tah ae ae call eet NY Bis 456 
UL OUTIFIAINETICON GM amt ae JOR ee ik ss vie oS v CRS Carve KAN eke iw eb eS SEN ES 118, 401, 457 
EOUIOLOOMCAT DB) CiS€aSe; DACIIUS 1GIVGE; cae. oa 5655 256s us ome a Seed Sa A 34, 273, 296, 297, 328, 329 
Mminesiesperiaum (oirvestn) (Hymenoptera; Platyeastridac) . 2.66.3. ss02sasnhet sates Sa enae OLY 127 
amoebae. (Class Rhizopoda] Amoebida; Endamoebidae) 5 24... 5 s.0 vines eee hagas bee ee oad 21, 40, 312 
Amyelois transitella (Walker) (Lepidoptera: Pyralidae), see navel orangeworm 
Anabrus simplex Haldeman (Orthoptera: Tettigoniidae), see Mormon cricket 
Anagrapha falcifera (Kirby) (Lepidoptera: Noctuidae), see celery looper 
Anaphes (Hymenoptera: Mymaridae) 
ViOVipe sa POLSICL Seer etter ene en. ws oe hee ed sy TOs a area Sins LAS REN ee ee 121, 140 
FO CICRALALLILEM eRe Sete eet ee AAT et he lich ca bles Ces GR RR TE we Oe a CE Ames 31, 63 
ovijentatus (Crosby & Leonard), see Anaphes iole 
Anarsia lineatella Zeller (Lepidoptera: Gelechiidae), see peach twig borer 
Anastatus (Hymenoptera: Eupelmidae) 
SDS RUSOMAMMNE eee Mes Gln i. CS a Ate rare EMMA IR ORME ven tha ea eeehs MENG SU a SSeS 419 
PICCESTIPT IT Cyst WALLIS eee tet re tn ami EE Ok ed ale wise ix Ee Cd ee MWY ees 419 
Anastrepha (Diptera: Tephritidae) 
ludens (Loew), see Mexican fruit fly 
obliqua (Macquart), see West Indian fruit fly 
suspensa (Loew), see Caribbean fruit fly 
Ancylis comptana (Froelich) (Lepidoptera: Tortricidae), see strawberry leafroller 
Angitia nana (Gravenhorst) = Diadegma laricinellum 
See OAEETI ONS CLAM TAOS LOIN OSU CPCI CHIE i Whee ntv'e pein n's.0\5 0 ee nl Eile + © wim) vie Viale a Won ale els Ullal ain 446 
Anisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae) ............. 6c eee eee eee eae 63 
DINGS OOLLOUT IEICE! COUSIELIOT CIOS UID ain 5 ei in clo in Cid ie a ees Dare lene de aid my clp old ays-aielshese siaiaie ate 6 104 


Anomala orientalis Waterhouse (Coleoptera: Scarabaeidae), see oriental beetle 

Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae, see Asian longhorned beetle 

Anthonomis grandis grandis Boheman (Coleoptera: Curculionidae), see boll weevil 

mMrOrdae anthocornd (Heteroptera) cit ceawuc se ewe cams lene tes RENIN ES 6 454, 535, 538, 539 
Anthomyiidae (Diptera), see maggots, anthomyiid 

Anticarsia gemmatalis Hiibner (Lepidoptera: Noctuidae), see velvetbean caterpillar 


587 


Antonina graminis (Maskell) (Homoptera: Pseudococcidae), see Rhodesgrass mealybug 


Antrodia ({Class Basidiomycetes] Aphyllophorales), see Poria .. 1.1... 6. cece ete eee eens 459 
carbonica (Overh) Ryvarden &.R.L. Gilbertson: 1.2 ays. ». Wilh Acierieb ates ate ee 464 

ants (Formicidae) ”{ .@S.Qui) hb-2 See See os ns eee eve eee 275, 286, 434, 439, 446, 448-450 
fire! Solenopsis spp SinU Wes een tes ces oe tea ey oo ca eee Nee ee ee we 54, 67-70, 275, 285-287 

Aonidiella aurantii (Maskell) (Homoptera: Diaspididae), see California red scale 

Apanteles (Hymenoptera Braconidae). (oii ati cei eet | oe Geet eee 417, 439 
forbesi Niereck®) We. aes eet ee slats wee el Groce, Phas wn ei te ieee ett ce eee 30 
fumiferanae Vieteck) (4.0 20 Sass Sees: oe eee Pete eae oles eae Ae ooh oy Oe eee eee 439, 450 


glomeratus, see Cotesia glomeratus 
melanoscelus, see Cotesia melanoscelus 
militaris (Walsh), see Glyptapanteles militaris 
marginiventris, see Cotesia marginiventris 
rubecula, see Cotesia rubecula 


(sens:.lat:)Sp. : . 25 aided Be aes be ei he Joe ae Reo BAe Pa a ge 439 
"solitarius," see Cotesia "solitarius" 
spp..(sers Late 2. Ce PP Hone Fe Dh res. MNS oe AE ete he a he 417 
Apechthis ontario = Ephialtes ontario 
Aphanomyces root rot of peas, Aphanomyces euteiches f.sp.pisi. 2) 20% 28 as 2a = ae ee ee 93 
Aphanomyces((Class Oomycetes} Saprolegniales)”. .... 2.4... onus ve veud¢alens siteo. 07 eo oon 4] 
euteiches Drechs. f. sp. pisi W.F. Pfender & D.J. Hagedorn, see Aphanomyces root rot of peas 
Aphelenchidae ({Class Secernentia] Tylenchida) i 3% +.).14, 422i 1. ges tetas re yea eee Vee 68, 536 
Aphelinus\(HymenopteraxA phelinidac) ss.2% 2a eek a ees bs ee i, ee 330 
albipodus Haayat'&. Fatima 3s. 0s ink sede 2 eS el ee, ee 138 
asychis Walketiid Hus. dces cB 2 ove 8 Bee < WES ee Oe we ee RE. cake Chee 138 
Varipes: (Eh OPSTET) mete Gina tate Ds, 5 Suh wes Hise wate eee seis SC ERB knee oes Cee Se oe rr 138 
Aphididae (Homoptera), see aphid(s) 
aphid(s)-Aphididacd sycs.gecio. os «ee Oe eee 10; 255,26, 30, 31)54,156-61 51248129, 34330 
arboreal yar rere» Sak Ae eal oc egret Rus a sd sole Ce I ee S758 560 
Cereal iets awk 5c Cee Rs. yoo & oars bvce < DARREN ORIEN Me ieee rr 4 ate ee 330)331 
C1 ee os ee aE cn MIA Da tM cc use ee es o 54, 58, 59 
pecan (includes black pecan aphid, Melanocallis caryaefoliae, blackmargined aphid, 
Monellia caryella, and yellow pecan aphid, Monelliopsis pecanis) .........00.0 0 ccc e ee ceas 7 
Aphidécta obliterata LU: (Coleoptera Coccinellidac) iim came ee ok) | eee ee 454, 538, 539 
Aphidius (Hymenoptera: Braconidae: Aphidiinae)i . 25. «. .  : . 5a: s+ qa a. neceen eee 330 
colémiund Viereck tui Oe aes ee Le oR eeR Se A eee 138 
Matricariad HAMGayir. test pei oo on ease ae oye sate eee micysonte hehe ioe heen Sel 138 
picipes' (N€eS) ie OR SO EER. Sd a ek 138 
rhopalosiphi DeStefani-Perézi sewed, Meh iey hs! SA i eae es ee 138 
uzbekistanicus WushetzKkita s220 ee Mee eee eb a.cin 3 & oe ce oe 138 
Aphidoletes thompsoni Moehn (Diptera::-Cecidomyidae) ow nc a. ens acee ones nae ps eee 454, 537-539 
Aphthona (Coleoptera: Chrysomelidae)@ 7.2.08 saver iiacse.o elec aienistee ay. oa. nee ane 85 
abdominalissDuttschmidt 270 22208 ei ces be ately oles egies 8 ee 85 
chinchihi: Chen ss 4.0 wos oh aso ied oa we le oe Pawk aay oe aR ee 85 
cyparisside (Koch) 5 cede. ci. bec pe sian ess 2 ss NY Oe eee eee en 85, 124, 141 
czwalintag (Weise) SAFES HEN Ss Soa ae es pee Rs Oe ee 85, 124, 141 
flava Guillebeau 22) 22. BREE Re ei. ee ee ee ee 85, 124, 141 
lacertosa (Rosenheim) {so 25%5.55. SERS SIGS An ER eee 85, 141 
nigriscitis Foudras Fake’ xo is Se rete d es eee oe ae Se ee ee 85, 124, 141 
seriata Chen. isi sadns 8 Fe pM bl Ciel ee ae a eee ee Ps ee 85 
Apis 
cerana Fabricius, see "Asian honey bee" 
mellifera Linnaeus (Hymenoptera: Apidae), see honey bee 
apple, :Malus spp.~.c% 35 ¥ 2 eae. BK ah eh terri > ee ee 99, 124, 327 
“apple ermine moth; Vponomeutaimallinellus 2s 22 eter susan ole tae ee 54, 55, 57 
apple maggot, Rhagoletis pomonella 2) 05 oss 1d scans ote 9 OO 24, 25 


Arachis hypogaea L. (Fabales: Fabaceae), see peanut 


588 


ania atc NG DIGelS IMLS ANCMICKS) ocd), 6. «3+ aussi nye ad 1. uate, dguiew a.ano Aap aiale.ore & a.euers 105, 113 
Araneae, see spiders 

Araneida, see spiders 

Arceuthobium spp., (Santalales: Loranthaceae), see dwarf mistletoes 


mE ids marmoraius (1 ownsend) (Diptera: Tachinidae) « .. . od. ccocc cis ant copgene ouage & eusene bie win ved Wine 9 wens 62 
Argyrotaenia velutinana (Walker) (Lepidoptera: Tortricidae), see redbanded leafroller 
ERSTE UNE at a i atis ve talc ELAT G10 my Eg 01 ole Baie Oe oI GP) eR CR i an 102, 456 


Armillaria ({Class Basidiomycetes] Agaricales) 
mellea (Vahl:Fr.) Kummer, see Armillaria root rot 


my Pere Pe, UNMET AA GG Sock aw cnc ww a se od Wes RDNA D aderbiay maw ape ae + Ad ge cate, s 456 

SS CAI a i Sone feacty 2 vcs « ARR choo oumebegies » +, 105, 116, 117, 456 
army cutworm, Euxoa auxiliaris (see also granulosis virus [GV], non-occluded virus [NOV], and 

EXC ean LES RN TS cs ere era epee a a). “and dais: sunt Suk, oe "oF sd esl SM aymiplcs wiepdumadunie se. 5 en 
SU VO CaM S CCC (al CLI LTT UMCL Cl eae Ae Pe feo ras ee a fac spss oad exegaies (SS G02 Bik hd scaynrdsiny as he oe 9506 4, 9 S03 Le 
Dire OSCR WSLLO Wem Gl Is UOSIOLCIISN. ts aay Min i SA ees me EEF «hs «GIP + WANE + HGyE vipers eee oe ee a vg 427 
Arthrobacter ({Class Bacteria] Actinomycetales: Cornebacteriaceae) 

Si ID Re ERE oa tele eigen 5 wd 9 BAG) See Few UAW ng wise oie why b, apa’ 117, 457 
aN NG) ere TEE TS COL) OILS mar me CMMs sabre) civ fy So ela © cae ne os effin 2 4.3 auaaege eel yn eutaayea oo #4 89 
Artipus floridanus Horn (Coleoptera: Curculionidae), "little leaf notcher," see citrus "root weevil complex" 
Pe OE COG oe Meare ee iN eT AEN Jee 97) sk 6 es sas eps of c0w 4 ooo MEE ole So Se os Spm aisle a age ee ® 314 
Ascosphaera ({Class Plectomycetes] Ascosphaerales: Ascosphaeraceae) ................. sence eee 325 


aggregata Skou, see chalkbrood of alfalfa leafcutting bee 
apis (Maassen ex Claussen), see chalkbrood of honey bee 


(EN Yo oe POSTER ES | Ga. 7S BS a ee er arg ar ere a2 
spp., see chalkbrood of "blue orchard bee" 

Bae Omnis eaten veloned DNA, VITUSES |, ASCOVITIGAC). . pc a5 hn ooo PRES oo cones buick ae aR 71, 289 
OW Ont cOriinealiy Olt) Mame manent un se fei aisle yar ves Sale 8 Gs a ana.die MOS alk S nocd ale « vibrate oie hedges 300 


ash, Fraxinus spp. 
white, see white ash 
ash borer, see lilac borer 


Asian 
SAP EO RIC CLEIIIECULEARPICAEALES Bo tated roc Fees) = Es Fate aie BIG oh cima hig shane ce ga PEN enter agrind ad 55 
"gypsy moth," see gypsy moth, "Asian" 
Beye c War Ir ISRCELUTIO Om re ats rhea el Gls soa SSRN aM raul e tans hadnt ain) sabe 275 
SlonoOMmed DeCUC AMODIODIOL 2 PIGDFIDENNIS oa suet fk cue Schon ty shih sss Futeenys tame ca. 0 es wat abies 147-149 
Pre ata arlemabert Ona AGC CISONCUia Pew nen. hol 5 ns oe 3 wwe nio'e 5 DO ne vl Sade ie 6 anes By Os 6, 16 
Bai AeA IDCLA) aSCG MISO THES SASINC Ginter, Gag cle sie aie oc win etia's a his se Wie cla pes eat hs V1 4 gobble Wie aaah egals 535 
asparagus 
POUICMBLOCHY COPY! G OSPATAQL 8, or 5 om <n itdls 19h) Oopdin oF p8,bueuhs Suohde igh RS axe gialoWiialhis aig din 3% Tra) 4s 54, 56 
De CHe MTC COr ISAS DOT IO iabe Mime Pr « acy sacha Bacclidahg © SPs Loess feo aire sec eve oy an aoa agen in 9 yo 15217 45 


beetles, see beetles, asparagus 
aspen, trembling, see trembling aspen 


Bote at SECT OGINES IND MMS rg ie An re fs Faso Diane RE Ce a Fala ulus oie Fas aang deop ts 5! mp bmi 9 (5 ajo ghd 273 
Aspergillus ([Class Hyphomycetes] Moniliales: Moniliaceae) 
TAGES Te GOT AT ol SINE Yates 2 ST | REPS ok ice nie SECC eee ae eC Ne eee deh 


Aspidiotus destructor Signoret (Homoptera: Diaspididae), see coconut scale 

Asynonychus godmani Crotch (Coleoptera: Curculionidae), see Fuller rose beetle 

Aureobasidium pullulans (de Bary) G. Arnaud [Class Hyphomycetes] ............ 0. cece eee eee ees 274 

Brier acne pig Optera PNOCUUIGAC) a cle ye silts sce one a eit He eee meen Sisk plein aoe taiendin (29a aaa 54 
californica (Speyer), see alfalfa looper 

Avena spp. (Cyperales: Poaceae), see oats 


B 
Baccharis (Caryophyllales: Chenopodiaceae) 
glutinosa (R. & P.) Pers., see seepwillow 
“Tali, 2 yo hu te ENONU) EN DRE DIG IMS Corse eas near i oer ee nae career Renee ee CATE PA 


589 


Bacillus ({Class Bacteria] Eubacteriales: Bacillaceae) 
cereus Frankland & Frankland’ 1887 222-223) e002 cn ot eae ae cyte ec oak) eel eget een momen B57 29) 
var. mycoides, = Bacillus mycoides 
coaqulans Hammer 1915, see half-moon disorder 
larvae White 1906, see American foulbrood 
mycoides Flagge:1886 ta 3. che. sinc ce te Statin «et eas Gen 8) Cle emia are eaters ar etree Lact eee 97 
penetrans Mankau 1975 ex Thorne 1940, see Pasteuria thornei 
popilliae Dutky 1940, see milky spore disease of Japanese beetle 


pulvifaciens Katznelson 1950, see also powdery scale ..........-. esse eee ete eee cette eee eee 274 
Sphaericus Meyera& Neide | 904 er eevee samie sre. vite eee sel enero ee ere one 284, 285, 320, 322 
subtilis (Ehrenberg 835) Cobre 1 822ae0ws wate tas one a oer eee eee 97-99, 322, 457 
SDPO cs cee te OS cee Cae te Mee Pe Mn ore cece scat 118, 159, 273, 274, 285, 322, 324, 429, 457 

Kylem-ColoniZing Pere We ees see see ches tc ele ae awe wh etl Pe ee 118, 457 


thuringiensis Berliner 1915, Bt (see also Bt in subject index) 101, 124, 126, 130, 139, 158, 159, 271, 272, 
276, 289-292, 295, 299, 308, 317, 320-322, 324, 327, 395, 414, 415, 419, 424, 428, 433, 438, 450 
alesti, see kurstaki 


Buibuistrain 25 hy Sieg ts VE eee a ee 414 
GAPINSTAGIONISIS OE eS ie en ie Gate Bk ek Foe Ie Suge Aa an COE 300 
PHULTIENSIS Re eRe se Se OUR TE CO TE se ce ae Thee OPE a Re TST nn eee 323 
ISPOCIENS ISOM Bre ee he OR rs nee Lee at eee ana TL, 72, 189,284,293, 295. 310,522 
serotype He 14 ence ie he ha elias ee ke tan ete ce ene ann ea nen 295 

RUTSTGKL ers ee eee Oar Ee INE care Se EEE eI eee One 293, 300,320, 3215 432 
PFDs PStrainiccc he cele O25 ow ARG oot ere TIE he eee nt ce Ce rece 432 

Od A191] Sea a ee ae eR ee Preis Saas gin or ants obio Gy Meee me - 321 
SQNGIESO. S248. ony hel Me Lista a5 Oy Wen Bes ec Sa SU, Sent g Sets earn oe) eee he 139 
ThUPINZIENSIS BRO A Ee ES Oe Ca eae Be Sone ee OR ar ee ce nae a ee ae 428 
Bacteria [Class] eevee ce ee ass oes peas ost teeter cae Oa tr 40, 320, 428 
Gram-negative®,.5 sos cre ypiines, pies Om ee Sica STEERER ey oie te eevee eee 273, 274, 305 
TOUS “hive Mae al dsc WN eM i ee aber ee eae ce She 213 
Gram-positive Aiea 32 ce bie aren oS SR ers ees ae eee ge ee are eae ee 305, 324 
Gram-variable pleomorphic: :..'\. 5.40.0 tame & cere Ree ok ee ee 213 


Bactrocera (Diptera: Tephritidae) 
cucurbitae (Coquillet), see melon fly 
dorsalis (Hendel), see oriental fruit fly 


baculovirus(es) ([Enveloped DNA viruses] Baculoviridae) ............... 35, 36, 70-72, 104, 113, 158, 159, 
270-272, 289, 301-304, 307, 308, 311, 318, 319, 437 

ACMNPV like 23 Oy os Gn Gee Ie te Se Lek se ect e eeee ee 280 
Genus A (unicapsid-multiple embedded polyhedrosis) =. %-:2.2.--2:06.2- 5 sane) ee ee eee 303 
Genus B (unicapsid-singly embedded vranulosis) <2. -.-. 5.12: estes ss tee eee ee eee 303 
Genus'C (non-embedded) ic-7 3. Sees eh Slee ele ae tee cs Se ee ee ete yee aren 303 
multicapsid/multiple embedded hee ore ta ete ot on ee eee eee 282, 300, 303 
non-embedded 5.2. 2a we Sa Le Be Pee ee Ae ees ae 303 
single embedded (See’also unicapsid)= a eee ee ie eee ee 281, 303, 318 


tmicapsid (see also single embedded). g20.005 05. . 4s: ete se ae ee ee ee ne 303 
Bagous (Coleoptera: Curculionidae) 
affinis Hustache, see "hydrilla weevil" 


hydrillae O'Brien g 35a). 255 oes wee ts Oe reer ee ek Snes Ree eee 86 
bagworm; Ihyridopteryx ephemeracformis <-.3..--..2 2. ee ee eee 308 
Ballia (Coleoptera: Coccinellidae) 

dianae MulSant \s.s% 0g deste 240 aie Ps So res ee 454 

eucharis Mulsant'y's ssi. 2 /nant Alias vlc 2 steer n pete ete eae 538, 539 
balsam 

fir, Abies balsaméa tA See Oe ee 447, 448, 450, 453 

woolly adelgid, Adelves piceae 0. 22544 ae eee ee eee 24, 101, 102, 116, 453, 454, 537-539 
“banana poka," Passifloradtripartita varomollissimd......%.1..5-. 5.400 0n eee 466 
banded cucumber beetle; Diabrotica balteata 3... 2.9.5. 2st eee 316 


590 


Bangasternus (Coleoptera: Curculionidae) 


areas CALLE tne MO et ace Ra, Clave Gg «a oadiiats acs y. Ste a 4 8 Do ge Aa b alyeblbarlehintoe 85, 86, 140 
Bret aL eh CEL NICOL UM ree eee tet atti oie he iacidstachc hy pas Gicditi allen bLa ve yd ly Ss ils ae AOEUN neh Saint 84 
Be eee RC ei te et ele Gi miad nies A SA «oid, vs, Bobs ghee hh BE ceal si acd WAV ss apa BiapeeMiew ah sidns 84 
ae OFAC SD Ren ee MCR Here eG Ct pik acs Fs nangee eA ls, Nie bistable patiegaiolauen® wie’ 121 
Boar eaters CRU OSTOS CATT ID COI OCIS mer rit en IMac aida so 5) c els ail G olaut nis ci ohe. x bie had hiegs He ecd\wainnisi'e * i 
Te rsOMTY COC S) | NS COIN ED TE | ere cee ees oa ole sce Rs SONNE, gia sa aid wil afal Slariiduedua 4 463-465 
Bassus pumilus, see Agathis pumila 
"basswood aphid," see "linden aphid" 
Bathyplectes (Hymenoptera: Ichneumonidae) 
CAPPER TLSa( 1 LO NUIS CML ar mie ey eae NE AP A Pes No a tat aVayalcsoccbous rbd Fintechun: + acullynsu gs, a 122; 138 
ECU TES Ce OULISON eter Pe tenet, a as ce ooo) a. <a cbpace beh my ihas Sahusnan ogi dliake! arate 30, 122.138 
REO NT LOM IED (dl OUISOLL) metee ee ee NE TM Ba cg se SM csr ache Meryl a oh 9 wg Agel iesdnaleounr mi cs o(dileaduns 138 
bean, 
RA UNV OU Ea COLES LOO? 1S ete eae ee ee Te Gaya tay vie iiss nF dcasiad weed Se wilt dc ine dba: oye 41,98 
ea SEOs LS CL OUIP LS Meme Mey Wee ae 1a 6 Te ee Dia ahi OA kh Sgt id SS pakeden AMEN klacgsd elo aac’ sm 127 
RAMI ILLS EC ES TV 11 LAE LS Mer nme oa eer eee Pee ra eae. af ec ¥in. a, eloo8 Sian wih aie dal aco ie, HSS 6).122,,124 
bean 
root rot 
black, see black root rot of bean 
ESC PITS HUIS IIASCOLL EY. terete AE oe ae cy als Gano ue wide - ony cratod etl til's Kaylactle ain le 4] 
Pere OGL ETE 2 SN) eee Rene RN ee at ner et. eS Wy Facts cts cata rmumand Wx Sim dia swialhythoe <c 93 
IRIS UMD OETT COMI DDETICICTIOULS Meats Senet ee Te ied oo. Site! co's la eos 006 8 eas yi am GCE aw Saeco 98 
Beauveria [Class Hyphomycetes] 
Basstaniel (aiSAM1O) osc ae. esi 34,35, 12; 124, 130, 13748805159, 2815291, 315.43.16,327, 414 
BA coun gg Sum ul Ay hee eR Pi) CRE oA ee Se 405 
bedstraw, smooth, see smooth bedstraw 
PRISCA WS MERTEN SOP Merrie ener a ne iy Pepi os 6 who A metp hae mache Ay: crieaP Adley aia « 83 
Peers inet y NEMO tCTAwT Dat are er ee tee VaR rrcrad Bicaes Slate vices eu al ven 69-72, 274, 305, 324 
"blue orchard," see "blue orchard bee" 
carpenter (Anthophoridae), see carpenter bees 
honey (Apidae), see honey bee 
eG EtsC AIO MG CCOCETING OCISEO HENLE tt. eae ai ent cle vavis soe wate eae ok Se aie Sepang page oierybesdssud 8 
beet 
BEINONOL UE SOOO ULETO CXIQUG hi ia sree oe giaiey tle ot fics Siegen teh Pa deh al ataliays iG cai oat es 29, 30, 282, 288 
cyst nematode, see sugarbeet nematode 
eelworm, see sugarbeet nematode 
ReaD PODM I CU CR ZCIIAIUS ae cetera aa hacets sia taie stole a's picts Gad etelm hee Manele nie ohh shoes tly eis. bls 8, 25 
Beenes( Goleoptevajy spay cc4 ess oer ee fee 4 24, 26, 33, 35, 51, 53-62, 64, 67, 68, 73, 84, 85, 159, 279, 305 
asparagus, Crioceris asparagi and C. duodecimpunctata (see also asparagus) ............... 51, 54, 56 
Bat CO VUGAC MeN res re Cort eEI eA: cies pyle eho gis 54, 102, 104, 108, 109, 110, 395, 402-409 
carabid (Carabidae) (see also rickettsia-like organisms) ..................... 305, 317, 418, 448, 449 
ReLai ounce eramOlClOde ere ht cee enn Gian o waren o5. 4 ea Chole sb cone armel ARKe dey 85, 396, 413 
checkered, see beetles, clerid 
CHEV SOE UI SOMeMUAS) wert cc a tr rier sso hain» ude aliyy waebecemncn pated Little ia siniel = fasall § 84, 112, 414 
DICE Cr CCN e) erie nr NT ee Usd Yooh ities ake Faceted ae a «,¢ dese ae ocuS WBE edi 108, 398 
click, see wireworms 
coleopterous postharvest pests (see also protozoan pathogens) .............. 6c c eee e eee eee eee 35 
SURE FOIGD? CLIC SDD Memnrtn: her ne ene ose nas GSE Uo els Shinlinlgiiniel Ope vim sodind Wun eee | 23507 
GETS LIIMCCUT ISON LO COCCI An mente he eatin ee Shes ysl hale 9 ws gusiy: wai ornie, sini Sele sos 327 
"dung" (Scarabaeidae, in part; scarab beetles that feed on dung) ..................005. 26, 54, 58, 64 
BCT Cray CAME S GDO Meret Se aetnr reN me rere eel yi 2. tate ed Se aie bik ail whasua im Saban Ania k + Bhs 104, 409 
Beilachnine (coccinellidge, subtam) Epilachninae) Ge. <<. ee es 5 cele so so dp rwtainysltin a roe ae die 24, 61 
ground, see beetles, carabid 
PSteTIOM FLIStEr IAG) rea eee oe Gry as a eli rit hh Vedran Wau’ sagen re pdlowin kale a aedeagal rel 58 
OORT UE LEO WINN 5c by ees Gee BGreg aa od EN OC ene 24, 67 
Pe areseera GEIDCCLICSACHIYVSOMENO Mr en ar ilon atau sn Genie Geers a need nls eae ena es 415 


longhorned, see beetles, cerambicid 


melyrid (Melyridae) ) ye 855 Ga a aoe lel a 8 ale ee tel osaletentia hel at te ieee et ene 427 
nitidulid (Nitidulidae) (see*also protozoan pathogens) nes. eine ene ee ener Sar 69.27 
rové (Staphylinidde)”? << 30%. Daye eaten teers creel slick w wlle tty as eg oo ee eee ee re 58 
sap, see beetles, nitidulid 

scarab (Scarabaeidae) (see also beetles, “dung,” and scarabs) 7.7... 3... ses e+ ne eee 316, 412, 414 


scarabaeid (Scarabaeidae), see "dung," scarab beetles, June beetles, and white grubs 
scolytid, see bark beetles 
staphylinid, see rove beetles 


white-fringed;'Graphognathus spp... $s. ices ces Sums ceue eo ee ee eee fee one peta etn terme 17 
Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae), see sweetpotato whitefly 
bertha armyworm; Mamestra configurata 0... sere td nls cue tere te meter ete 327 
Bertsenus brachycephalus (Thorne) Massey ([Class Secernentia] Tylenchida: Aphelenchidae)........... 536 


Betula spp. (Fagales: Betulaceae), see birch 
bindweed, field, see field bindweed 


Biosteres arisanus (Sonan) (Hymenoptera Braconidae). 2.7... we Se ee ee 63 
birch, Betula’spp erik: Fees sce SS ee ete he de evs we ee ea Pet ee 106, 162 
birch leafminer#/entsa pusilla weo-5 niet ogg tno ramen tetas Seae ee saree eee ae 42, 54, 56, 58, 60, 162 
“birch leafmining sawfly;" Heterarthrus nemoratus® 2.5 $005 S26 bore Hass Ane ne 8 
birds. [Class¢Aves| oe xterra onan ore ete ae 36, 396, 400, 413, 434, 436, 439, 444, 446-449, 463, 466 
“biting lice,"““(Mallophaga: various families) "2.\.0..2. .ee.acet ts tv ee g21 
bitter rubberweed; Hymenoxys odoratat 7s. ae aie ne oe ea re Le 81, 82 
“bitterweedsS' HyMenoxys SPDo- cars ee is wie Bie cag gt Pema Ne aE ee ee ee 77 
black 

imported‘ fire ant} Solenopsis TIChteri Meee leak Se re ee Ste Ae eth 285 

flies(Diptera? Simuliidac) 27... / shee ee Re ee atelier 284 

pecan aphid, Melanocallis caryaefoliae, see aphids, pecan 

rootrotof bean, Thielaviopsis basicola wins Aosta ee oe or es a 93 

scurf of potato, see Rhizoctonia scurf of potato 

turpentine beetle; Denaroctonus terébransis, 416 ned ae oe ee 102, 104, 107, 108, 395, 403, 406 

Walft,JUGIGHS IGT ALIN oss fi. ov alle Fae nee yk Sate 2 EL AO one eee 415, 462 
“black Stales;"Saissetia Spp Mrs: <<a. m0h ices ee ck Weak i nee hows asian REA oe eae eH 
blackberry; Rubus Spphy aaeh eI, Ss oO dite oie het nal NO ee eee nr 466 
"blackhéaded budwormy' Acleris'Varaing ceue «a. eontca ss g ce mee ee 438 
blackheaded'pine'sawily,)Neodiprion excitans tem sss < an ta ee et ee 113, 432, 433 


blackmargined aphid, Monellia caryella, see aphids, pecan 
Blattodea, see cockroaches 
Blepharipa (Diptera: Tachinidae) 
pratensis (Meigen) “Pe Bee en ee oe de ee a ee ee eee 103, 111, 418, 419, 422, 430 


SPP.” PoP REE ee hee rice ce STS SOR we Gat 4 wes OEM tote > SER anne ee cee 421 
Blissus (Heteroptera: Lygaeidae) 


leucopterus leucopterus (Say), see chinch bug 
spp., see chinch bugs 
blister rust, see white pine blister rust 


"blue orchardibee;" Osmia lignaria propinqua 0220. oe dnae 4s ee ee tee 324 
blueberry, Vaecinium sppiieon re ere. A ae alte Se en et 99 
blueberry maggot; Rhagoletis mendax: <i. 524 hasta ce ek eons see nea eee eee 25 
bluestain fungi t Srey SSE A ee or Ne On ag tee ene 407, 408 
Ceratocystiopsis ranaculosus —0..:812 oo Ieee ie Op ee nas on ee ee ee 408 
Ceratocystis coerulescens*). a: Sth cas de one pepe eG ee ee 465 


Ophiostoma minus, O. multiannulatum, O. piliferum 
boll weevil, Anthonomis grandis grandis (see also 

protozoan *pathogens)“3. 4245. 20 Se ee 7, 10,°30,35, 62, 63, 65,71, 72. 12 ee 
bollworm, see corn earworm’ W266 os 5 6 65 caee wus web ao eve wales » Ee 26 
bollworm/budworm complex, see Heliothis/Helicoverpa complex 
Bombyx mori (Linnaeus) (Lepidoptera: Bombycidae), see silkworm 


592 


borers (see also in subject index) 
shoot, see shoot borers 
stalk, see stalk borers 
stem-, see stemborers 
Botanophila seneciella (Meade) (Diptera: Agromyzidae), see "ragwort seed fly" 


Pr eC ere et ae el CLAS AY OD OMOCCLCS IWR time Ra Mie [ole duc cc 4 dose hv nem cits 6 6 nn eas wee anes 98 
Bovicola sp. (Mallophaga: Trichodectidae), see "goat louse" 
bovine contagious pleuropneumonia, Mycoplasma MyCOldeS 5.0 ie oie nets ne tine che en nes anaes 306 
Brachycorynella asparagi (Mordvilko) (Homoptera: Aphididae), see asparagus aphid 
Brachymeria intermedia (Nees) (Hymenoptera: Chalcididae) ............. 0.00. cece eee eee 103, 419, 422 
Bracon (Hymenoptera: Braconidae) 
Tie At ee Er ge eee ae ahs teas o) 4. 09 gatas! amy Qusuhldian a ‘aap «0-2; supra sas. -<c0, ©, 60 63 
te at ae ee em te ed ee I reall PU ePIC S™-8Ygo aE Maiabtiece ers sa + 0 deere ¢ doe 20 30, 65 
Braconidae/braconid(s) (Hymenoptera) ..................05. 148, 396, 397, 401, 410, 419, 421, 430, 535 


Brassica (Capparales: Brassicaceae) 

oleracea L., see cabbage 

var. acephala DC., see collards 

spp., see cole crops 
Brevicoryne brassicae (Linnaeus) (Homoptera: Aphididae), see cabbage aphid 
Fy Sul GUS a) Gate OMA LAR) oe MUN ong Oe ec Oe 30 
brome, downy, see downy brome 
Bromus tectorum L. (Cyperales: Poaceae), see downy brome 


Pcie AN OG POO Ca TICLECTZIO SV OUINCIC wrens ilps I Pe gg sox aden ton hv dg dugde a oED. 18) a) 8 bas) aoe. e wae 81 
broomrape, see hemp broomrape 
SRST INSITE AOE Oe R 9 Sede een eG Oar act ge ee er 77, 82 


common, see common broomweed 
Texas, see "Texas broomweed" 


brown 
GEIENST Oe hOLO PCr ONC IC! Ok mete APIECE I 6 Sie. ick sym wate iaiis no wn 20M Spee A + Guin eBeamnenoncalne ae dl peoviaie 149 
rot 
eee eS a) LOTTE AI, (7 CEICOL PRP iS ols Shs 8 ois ny apoehS ea ied CoeUgded tre KongS PSY gyake wide idnn 98 
of wood 
GP TESTING TON ESTE TH Gl. 4 eras See Sah RO FoR RS OC on Ee Oe ne Ot 1 ea aa 463-465 
BVO CHILI GH COIACTIC MRR et ie eke Noh A AE iad cel Meco So, AD yaionvan BU eeSix Wi alia ve ol Fag 464 
Postia placenta, Antrodia carbonica, Coniophora puteana .............0 eee 118, 464, 465 
RNR AROS OCI SITES CTI IIIS MiP dep noee es 6 og de npc eyes, oo haa attain picaletade na legis. dhols, is, orally» Sey 
Bec OL UDMOCIS CINVSOMNOED oie oA Scene sulk Cos ence N debe eye eee eee ees eo ale Lod 
ery sict SUTTON ED Wt SECIS) TO WIM AINSTIOUN) Mepis ge aes Exayurvice >: dps gitle idan propa @eh aya Tavis, senahs soqdyegs a3 6 0 7 


Bruchophagus (Hymenoptera: Eurytomidae) 
platyptera (Walker), see clover seed chalcid 
roddi (Gussakovsky), see alfalfa seed chalcid 
Bruchus (Coleoptera: Bruchidae) 
brachialis Fahraeus, see vetch bruchid 
pisorum (Linnaeus), see pea weevil 
Bt, see Bacillus thuringiensis (see also Bt in subject index) 
Bucculatrix thurberiella Busck (Lepidoptera: Lyonetiidae), see cotton leafperforator 


OM SGERERCLEDTE NS ooo Gah PV gy Bg) 0 sane, Ti re ee a a ee oP 102,105, 115 
Burenella dimorpha Jouvenaz & Hazard (Microsporida: Burenellidae)..................... 0000 ae. 286 
Bursaphelenchus ([{Class Secernentia] Tylenchida: Aphelenchidae) 
NPIS ORE VIR WE NANO) OPGCS EOS ae ceric i er Ae oe a ra 536 
Beer ee an RENO Ns OOO a Ny es pah nc acted fa eds dedny ope matali, dickens acount aca ayes fein 8 536 
buttertlies (Lepidoptera; in part) (see also spiroplasmas) .... 2.2.22... see eect e ee eee nee e eee 305 
C 
cabbage, Brassica oleracea L. (Capparales: Brassicaceae) ...............-20005- 25929) 31, .32:299)309 
lemiddemtencusipests Ofna weil nrht Lis | oP eed Lisl. WWM tae Bale ele old ee 25, 29532 


593 


cabbage 
aphid, Brevicoryne DrassiCae sowie cd Gs ee oe ee obnain ay vie es ee Pie ae ie oe 3] 
looper, Trichoplusia ni (see also cytoplasmic polyhedrosis virus [CPV], multiply-occluded nuclear 
polyhedrosis virus [MNPV], nuclear polyhedrosis virus [NPV], singly-embedded nuclear 
polyhedrosis virus [SNPV], polyhedrosis virus, and RNA virus) ...... 29; 29,30, 51. 35.7 U0 aes 
158, 159, 271, 281-283, 288, 300, 302, 308, 309, 317, 318, 452 
Cacopsylla pyricola Foerster (Homoptera: Psyllidae), see pear psylla 
Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), see cactus moth 
cactus moth,.Cactoblastisicactorumm™ con. co. oe els eee aie nt ge oie eee 280 
Cadra (Lepidoptera: Pyralidae) 
cautella (Walker), see almond moth 
figulilella (Gregson), see raisin moth 


éalici-like virus (poss. Caliciviridae){¥ a. ies & acosene so Ayes ee Aree Poe een ee ep eee 280 
Caliciopsis arceuthobii (Peck) Barr ([Class Pyrenomycetes] Coryneliales) ............... 0.0.0 eeue 466 
calicivirus: (Calicivirida) sigue son sfie cece «ek es eins <a an oe fe ean eee re ee 10.2 ode 
California red. scale, donidiella. aurantlin,ccckamerien 6.08 ice snc wie ee ee ee 24 
Calosoma (Coleoptera: Carabidae) 

S Pins Aeyails eke Reiantis ani ee ne ok the nas bas gs crocs Soe pane Slate Caren ae eee ee 418 

sycophanta, Lng asa dxtsantuns delay tee abate: the nn os etn aly ae ae te ree ch 422 
Calvia sp..(Coleoptera: Coccinellidae) oi 2.20 55.0.-: S28 soe eee oe te ee 538 
Campoletis (Hymenoptera: Ichneumonidae) 

Jlavicincta (Ashinead) cet ecitetean oop 6 aa ane oe Si Sore ale amt oti Ok ori ee en ee 30 

perdistinctus, see C. flavicincta 
Camponotus sp. (Hymenoptera: Formicidae) aan, sac ee ne ee ee ene eee 434, 449 
Campoplex frustranae Cushman (Hymenoptera: Ichneumonidaé) 2... 2... a. cs oe eee 411 
Canada thistles Gisiuniarvense. «oe. 6 a erate siete eee a oe See Tae 36, 37, 0s 
Candida ({Class Ascomycotina] Endomycetales) 

guillermondii (Castellani) Langeron & Guerra’. (55. oe aie eee 98 

oliophila Montrochetsa\:. cut) oP aciiataeeicee <a sce te ene ee 98 
cankerworms. Alsophila.and, Paleacrita sppajn «se toe soe cee etl ie. eee ee 102, 112 
Caprimulgidae.({[Class:Aves|Caprimulgiformes) “22 ieee eee a oe nee eee ee 536 


Capsicum spp. (Solanales: Solanaceae), see pepper 
carabid(s)/Carabidae (Coleoptera), see beetles, carabid 
Carduelis pinus (Wilson) (Passeriformes: Fringillidae), see pine siskin 
Carduus (Asterales: Asteraceae) 
acanthoides L., see plumeless thistle 
nutans L.', 
subsp. leiophyllus (Petrovic) Stoj. & Stef., see musk thistle 
subsp. macrocephalus (Desf.) Nyman 
subsp. nutans L. 
pycnocephalus L., see Italian thistle 


SPP dicans Aneta ists She) cand ait aah Weel Fhe ord gee Age emt ee eee eee ae een 83, 88, 89 

tenuiflorus W. Curtis, see slenderflower thistle 

thoermeri' 
Caribbean fmt flys Anasirepha suspensa nee oe ee en ee ee Ge ee 68 
carpenter bees { Anthophoridae) see also Xylocopa .1 >. 5-4). -e eee 275 
carpenterworms.Prionoxy situs robitide) a ae nc ee er oe ee ee 68, 278, 413 


Carya spp. (Juglandales: Juglandaceae), see hickories 
Castanea dentata (Marsh.) Borkh. (Fagales: Fagaceae), see American chestnut 


' The correct taxonomic name to be used for the majority of musk thistle populations in North America, 
according to the rules of botanical nomenclature (J. H. Wiersema, ARS Systematic Botany and Nematology 
Laboratory), is C. nutans L. subsp. leiophyllus (Petrovic) Stoj. & Stef. (= C. thoermeri Weinm. sensu Kazmi 
[1964] or McCarty [1978]). See also Moore and Frankton (1974) and Desrochers et al. (1988). Some releases 
against musk thistle in Montana and Texas, and some collections from musk thistle in Italy refer to C. nutans L. 
subsp. macrocephalus (Desf.) Nyman. 


594 


Rese eat CE eOCOMMOLT SO armen N A ty She clay 4 dk ho ale aks ak FA dieu diel ove bon ein wwe 443 
Sasinaria mieripes Gravenhorst (lymenopteras IChneumonidae) ..j. <6. 5. oj mne ose nlavn agen” & dokeviceelaged nas Ades 421 
Cassia (Fabales: Fabaceae), 

obtusifolia L., see sicklepod 

occidentalis L., see coffee senna 


eat flea, Crenocephalides felis,(see also rickettsia-like organisms) joc... ose ajece 9 2s, 9 sabe veyeye a sha ala eas 301 
matane parceseiosa (oicard) (Coleoptera, COceimenidae ye acca sete a4 vos s4ryonepanechde Synneuenn. «Ke © wloinounme 130, 137 
Oclenarigsh (| Glass Cnytridomycetes| Blgstocladiales) temic +4, 2% &cpntsscnes eae’ vie spsragesie. 8) Sopnnspainua cna sualenare 40 
POMIACCUS PTAnGIS BULKS )ALLYIMeCNOpteta, PIClOMANGAC) | oo aicc cc ce ies balsa cing ve Sele e Glan ees 63, 65 
eer Leae NLS art) OR CLIC S OU) eam uO gE eee as ea Ae hoya tn andy ica sv'onn ins dpas's ssh bin nre: psoeheaupiiey AEE sey 322 
Bec Ct Vide CECICOUIVIIG LAD tend) Me mtmn mente man tes alate reals & ha de. 4 fgl a kh w els ¥ ds fateh Shale 454, 537-539 


Cecidostiba, see Dinotiscus 
celery looper, Anagrapha falcifera (see also multiply-occluded nuclear polyhedrosis 
Vitus NEY land nucteal poly begrosis,VitUS LINE V ] inane cccudian sine? sate to oH beacause 72, 280, 308 

Centaurea (Asterales: Asteraceae) 

diffusa Lam., see diffuse knapweed 

maculosa Lam., see spotted knapweed 

solstitialis L., see yellow starthistle 

spp., see knapweeds, starthistles 

virgata var. squarrosa (Wilde.) Boiss., see squarrose knapweed 
Cephus (Hymenoptera: Cephidae) 

cinctus Norton, see wheat stem sawfly 

pygmaeus (Linnaeus), see European wheat stem sawfly 
Cerambicidae (Coleoptera), see beetles, cerambicid 
eran samarcnsicn vy uieneuve) (Diptera: Lachinidaé) 2 .2.% . 2 5 ctw «seyssapestacvoaiseemrs(e's. aw McayeeeSboers 12d 
Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), see Mediterranean fruit fly 
Ceratocystiopsis ranaculosus J.R. Bridges & T.J. Perry ({Class Pyrenomycetes] Ophistomatales), see 

bluestain fungi 
Ceratocystis ({Class Pyrenomycetes] Ophiostomatales) 

coerulescens (Miinch) Bakshi, see bluestain fungi 

fagacearum (T.W. Bretz) J. Hunt, see oak wilt 
PerCUSO a lealsporor peallt, CercOspOrd GFOCHIGICOIA on ies eh oe eid a 2 ds 2a,» Gadgarpemd hep ms) key 97 
Cercospora arachidicola S. Hori [Class Hyphomycetes], see Cercospora leaf spot of peanut 
cereal 

CV SUC ALCe ECL ENOLTG AV CIC Rice ns tall Wal sdk deer inlitis. wilinn Beacons <pan'y « fupccdy Caudalie: asedinkys a2 

leaf beetle (CLB), Oulema melanopus ......... 2420, 30,42,53,.50,.120, 121.125.140.145, 157, 161 
Ceroplastes (Homoptera: Coccidae) 

cirripediformis Comstock, see barnacle scale 

floridensis Comstock, see Florida wax scale 


Certhia americana Bonaparte ([Class Aves] Passeriformes: Certhiidae) .............. 0... e eee eee 536 
eeriniiciad (1 ClasstAwes LE ASSCliOUNES ema da ceac mics Vas sas the bin Ras v4 es Sumapniele egeastott Wx 536 
Chaetorellia (Diptera: Tephritidae) 
DLrolo mia nite oes yar Ual Ub ae see ys uo nigtasds Gece Pi ails, » wie Pamhs ae R Gy eapRlensy o's: 86, 140 
FAIS TEES A CCD Meme ace Fa es ore Aaa aes. ony. -c tel 2 oye, MaMa eiietinniel iiach « giecictel dio ach sha say eacesays 84 
Pralciioiad uymenonterasuperramily ChalcidO1dea) nie awe ees oo yne's 447s wo Peotone phwimtaw) fra Ph tethers 446 
Ba KMTOOd aS CO;DI CH IS I) Mma Mea. St tea nua ens, cchniss BS bare 3 VG mtr aint oe aig. ches mrecegalats 69 
of alfalfa leafcutting bee, Ascosphaera aggregdata........... cece eee 34, 70-72, 159, 324, 325-327 
Orne Orenard Dee A SCOSPICEL GC. SDD acm a tees tra cya th Neen inch Sita nde WES sf a Salli dixin eh we sean 608 324 
Cai DCC ms ce MN E ei ei cee a oleae. he eis aye a ee echoes tie cchbreraie f © atewend 34 
DE NOREVEDCGEA SCOSD GET QD IS ra Bicre cise cis 4 ure,» ts aud width, 29% poked Diopcl 69, 71, 159, 274, 275, 326, 329 
Parainipeniyildae cial verily UC (LIMtErs ae dlseeua iis Wists wil 5! «\s 06 om Hore eisiells wip ty'suenela elo sis my 453, 537-539 
Chamaesphecia (Lepidoptera: Sesiidae) 
CSS ICONS at 2 lee eat ee ee wi Oe Pe ne bce, oho v Ma qgiedinnttegeysjayes aie dace wang ahd 85, 141 
ICU ICO mala i eee Bee tae nie EMail visi ie | ars. o o = 2's 919. «de giakeerBaysgrns ely oe shes) s/he 5 85, 141 
TERIDT CGI Or mis Mi Cis Go oCiItterMUllel) ah greet ecni es chs as ve sip steh ad edd eo 4344 mo vy wee 85 


Chaoboridae (Diptera), see phantom midges 


595 


cherry 
fruit fly, see cherry maggot 


maggot (also called cherry fruit fly), Rhagoletis cingulata .. 1... 0. cece eee ences 24, 25 
chestnut, see American chestnut 
chestnut blight Cryphoneciria parasitica Tancwe wot 17a tee 0 eee a ee 105, 117, 456 
Cheiloneurus inimicus Compere (Hymenoptera: Encyrtidae) 7070... 0 0 en cient enene «ees eee ems 31 
Cheiropachus colon (Linnaeus) (Hymenoptera: Pteromalidae) ............0...-0 ste tise teen eee 402 
Chilocorus kuwanae Silvestris (Coleoptera: Coccinellidae) a s2 200. oss eee ee 59, 124, 140, 539 
chinch 

bug; .Blissustleucopterusileucopterus (662s ogee lates aes ee ee, aan gre ee ee 11 

bugs! Blissus Spps seat Eee RAR eo Poh PWR ATES Mig Oe aes Daca i eee or eee 61 


Chondrilla juncea L. (Asterales: Asteraceae), see rush skeletonweed 
Chordeiles ({Class Aves] Caprimulgiformes: Caprimulgidae) 
MinoPEoTstery fo TF OIN SO SE AA POOR eee eee RETR cee ole 9 oe yee 536 
spp., see nighthawks 
Choristoneura (Lepidoptera: Tortricidae) 
conflictana (Walker), see large aspen tortrix 
fumiferana (Clemens), see spruce budworm 
occidentalis Freeman, see western spruce budworm 
pinus Freeman, see jack pine budworm 
spp., see budworms and spruce budworms 


chronic 
bee paralysis. virus (poss; Picormaviridaé) 4. oA0ce ene tee ee ne oar eee tere ee ee 297 
Stuntvirust possh Calicivinidae) iar s oe 5u5, ae ee gs Ee See Ee ee ee 7102299 
chrysanthemumy Carysanthemunt sppitnnss. Wes te ees eos oe oe ee en ee ee 94 
Chrysanthemum spp. (Asterales: Asteraceae), see chrysanthemum 
Chrysocharis laricinellae (Ratzeburg) (Hymenoptera: Eulophidae) ......................04. 15, 440-443 


Chrysomela scripta Fabricius (Coleoptera: Chrysomelidae), see cottonwood leaf beetle 
Chrysomelidae (Coleoptera), see beetles, chrysomelid 
Chrysonotomyia (Hymenoptera: Eulophidae) 


JOrMOSA Westwood) RE hex Pe Rae Os aor, od «ek GRMN cn aie es Ne he ee 114 
ruforun? 6 ausse) 5. 25 eee Oe Te ae ke nee. ck et acy ene eee 114 
Chrysopa (sens lat.) sp spp. (Newropteras@hrysopidae) "7.2" .. ean. s ek ee eee 454, 538, 539 
Chrysoperla QNeuroptera: Chrysopitiac) to nee oe ik nee eens cis. cee ene ee ee 61 
carnea (Stephens), see common green lacewing 
Fes ADFis*(BULMeIster )ESRes See ttre Sette eee, Sah ee eee Pree cee ee 61,562,139 
SPP Pr raton!s 5 save ahete bik yl ane cae men Weel ge en oa ey Sage i eager ne eee 62, 65 
Chirysopidae/chrysopid (Neuropterda) 2055 seas Gee ee centre te ee ee ee 338, 539 
Cicadellidae, see leafhoppers 
cigarette beetle; Castoderma serricorne: in. sn oo oe eee ee ee 3D 259 


ciliate [Phylum Cilophora] 

tetrahymenine, see tetrahymenine ciliate 
Cinara (Homoptera: Aphididae) 

cupressi (Buckton), see "cypress aphid" 


subinaetGillette’&:Palmer) map see ssh s4e Sees Se ee ee ne ee eee 455 
Cinnabar mothyiyriajacobaeae ik BABh a tae sme. f4 ta Gao ta aus Sec UAT ee ee 38 
Circulifer tenullus (Baker) (Homoptera: Cicadellidae), see beet leafhopper 
Cirrospilus pictus (Nees)(iymenopterarEulophidae) 22,255... 0.6. ee 440 


Cirsium (Asterales: Asteraceae) 

arvense (L.) Scop., see Canada thistle 

spp. (native north American thistlés) 225-2270 2 ond eect ee ee a a ee ee 89 
Citrus (Sapindales: Rutaceae) 

Jambhiri Lush., see rough lemon 


Spp., citrus(see also spiroplasmas) 4... ete ee 24, 29, 31, 32, 57, 68, 98, 283, 287, 288, 305 
citrus 

blackily, Alewrocanihus woglumi -......... even ti ee 3,9, 17, 18, 24 §20, 17 

canker, XarithOMONGS CUPL. eo a ee nine es oe ok oss eee Oe ee ee , 267 


596 


recites anonyenus ciirt (see also non-occluded Virus)....u sn aka os eee eee. 35) 2824283 
"root weevil complex" (consisting of the Fuller rose beetle [Asynonychus godmanil, "little leaf 
notcher" [Artipus floridanus], the "citrus root weevils" [Pachnaeus oplaus and P. litus], and 


the "sugarcane rootstock borer weevil" [Diaprepes abbreviatus]) ...........0000 cece eee 287, 288 
PUN GERTE ICON IE?) MICO DIT CIO CI UOP CA ely teas tei 4 Sad heh pos SIL) AAR MR We Ae ee we AE 287 
RNATUIC VEDIC CHILO COSSOUIT anthro es ir oh ala, Silvie Shs WR Seon SEARO Daas eet Bianca N23 e128 aN37, 
(ONE SEES SEG d DO ERTS 8 Vi el Teen dha Lote MAE fe: race Aero, een ee en ce 94 
OUEST ATSC UG Ho foe OCTET! Rie a rots cea. ce 02 ne Ae No a ee eT rere 413 
mmasedeoreoniena ) see also peetias: CleriG i cu. <a de w dso sa, is Web ch e tealers FcR ek sad 535 
Clidemia hirta (L.) D. Don (Myrtales: Melastomatales), see "Koster's curse" 
clover 
Te A OOS EE CROC Ota ret Cea ae) oy. a Pa odd Ve « DEM AMMEN EN EW. BSG a OT 128 
ROG CiCnAC er uCHO nNOS PEA DICE see the ake ea ace Riek Med Rees Se NSPS ae. REM E AN 24 


Cnephasia longana (Haworth) (Lepidoptera: Tortricidae), see omnivorous leaftier 
Cnidocampa flavescens (Walker) (Lepidoptera: Limacodidae), see oriental moth 
Coccinellidae/coccinellid(s) (Coleoptera), see also beetles, lady ... 104, 128-130, 137-140, 414, 454, 537-539 
Coccinella (Coleoptera: Coccinellidae) 
septempunctata L., see sevenspotted lady beetle 


Man Vers Mtn Om AMUN IMAUC ine pce os Ck 2) Ouion es aineeeyn + lodhels 4 ¥SARAd MS 137, 
Poccimellinaoncoralis (Germar) (Coleoptera? Coccinellidae) . .... 5 no eee sos see Pia ale s oa Ha slaves 137 
Coccobius sp. nr. fulvus (Compere & Annecke) (Hymenoptera: Aphelinidae).....................04. 140 


Coccoidea (Homoptera), see scales 
Coccus hesperidum Linnaeus (Homoptera: Coccidae), see brown soft scale 
Coccygomimus (Hymenoptera: Ichneumonidae) 


isPGr eV ACTECK \ME eee ee ts, Ste nl te Ge 259s I . RY SA OS ee 59 
Cochliomyia hominivorax (Coquerel) (Diptera: Calliphoridae), see screwworm 
OC COUN e271 e SDD a aerate noah cee pu tacialielmocie lh Gulva.s eva w aauincs wo eelbleees wheal say 77, 82, 89 
COC OAC Resi Dy attOcea ier awe ciirnr wre he Pa ee, PA oe ce. 5 Sealers Sailing wane a acid o WM RO OS Hn 54 
Eve (MRCOG St AIS CSIP AIC TON et use ee ae eng eel einen ene ee oes Eee ECHR A leh ORT A OS 16 
codling moth, Cydia pomonella (see also granulosis virus) ............... L359 17730;33;54.51589327, 331 
Coeloides (Hymenoptera: Braconidae) 

rr erIRAOITON TOC CC me apn Re ef cos sty vans o ivls, wis p¥ oem Sad em 4, SA 6 AEH wid Dem HA Se w hm wale 108, 396 

Per OC WOT MOUS IITA) Mma Pee are, path, shanierauex REPO E ROR OR: Me A ame et. £4 397-399, 535 

ST) ea MMe Paco nih gc orgs Joncas adhiehty Stand Oe shins, Min A RO NS Malay aioe, OL AA RS 397 
Coelomomyces ({Class Chytridiomycetes] Blastocladiales: Blastocladiaceae) .................0.0 005. 294 
REI CARCI AM aes ICIOCCIOCHIONS ane ak eeeh epee A Ae cn s .8.58..5s eta alta lathe bs 0. 91 
Coleomegilla (Coleoptera: Coccinellidae) 

niaculata(DeGeer) eaars sas): eer pet Ce aR OS rtettndS.. 1 iS. See ad 110, 128, 139, 414 

PURE Ar TRAC CLIOEMNCTO ete ges Se es ay apek Weg: ics yo Goan AMMAN ie AO CN th 3 SD 137 


Coleophora (Lepidoptera: Coleophoridae) 
laricella (Hiibner), see larch casebearer 
malivorella Riley, see pistol casebearer 
spp., see "casebearers" 


@ olecptera/coleopteran(s), see also beetles ic weet Wiig. acne oy we eens oman 276, 303, 395, 396, 413, 415 

See RO TIN VME mE CSL ePID) Mn PR SE a pil. enna (S-GE A st Mibegia tie OsoNts pear to meek dg od eae rien Bla RSs 25,34 
Colias eurytheme Boisduval (Lepidoptera: Pieridae), see alfalfa caterpillar 

Colorado potato beetle, Leptinotarsa decemlineata (see also spiroplasmas) ..... 51, 56-58, 60-62, 67, 68, 123, 

1287 129,139 1469147, 278; 292, 299, 303,305,315, 3277415 

SOIT OSMDLGStICOIONC  ACGUEN lA ACCP Al Cima t ria elias ha nde e tl A eau tys WRG wee ewe ee os 302 

Colletotrichum [Class Coelomycetes] 

Pioeasponioidesheuz)) Den sooner IE CNZ, wan ia fee ine rar yele Sas, -n nln gt aieee eye 8 ala 9 ae 466 

PR SOMCHESGITI TIOMHEISCACELTIN) BET grit rere ne ch a De 6 ee hc: PARTS oS as PTS 88, 91 

Ponce oa tecuweln, PANGS cc W 1D) MOOG gpd eee eye eae eae vee deans as 89, 90 

ollyria covator ay iliers) (aymenoptera. Ichneumonidae) oo... ee ete eee eet ns 16 

CONT ORIG WE OEE EY) os cine wees Stn IG Pio i HIN ean Cl ainc are Roa ce erence ee ee a Se) 

BOMiMOn DLOOGIVOCO CI ICITEZIC ArOCUNCHIOIGGS 2. cece co ee ete OMe ene we ee ene emer eb eague 81 

common green lacewing, Chrysoperla carned .......0 16sec cece ee eee eee eee e ees S271 02100, 291 


597 


common"pine shoot beetle," Tomicus piniperda ...... 06.6. cece eee eee een enn es 106 


common purslarie# Portulaca oleracea: 000. 10. coed Re Cael fies SINT DRIES. IGP ie devs ene ne yee aman rn 78 
common scab of potato, Streptomyces scabies. 5... Oe ie ee in Te eee se 13, 41 
common St; Johnswort/Aypericum perforatunts neon og bn e akrules te ities Sones 21, 36, 83, 146, 161 
Compsilura concinnata (Meigen) (Diptera: Tachinidae) .............-..++-e ee 103, 420, 422, 423, 430 
Comstock mealybug, Pseudococcus’COMmSIOCKE 50a ais ions s ok ees ele 16, 18, 25, 161 
Conidiobolus ({Class Zygomycetes] Entomophthorales: Ancylistaceae) 
coronatus (Costaritin) Bathoo : 200 ss Are ied Se a aims ie het aa adm eleva nde lea 284 
obscurus (Petch) Remaudiére:& Keller o.c55.< 26. fis c= wiv ou octane ou iaaliek nelle acl ole ars meet ane 314 
thromboides Drechslet” 622.5), 00V 2 SIA OI el 314 
Coniferophyta, see conifers 
conifers [Class:Coniferophiyta ices eames 6 ae ar coe eee Bm ered rom wa) oe 414, 416, 428, 432, 454, 459 


Coniophora puteana (Schumach:Fr)P.Karst ([Class Basidiomyctes] Aphyllophorales), see brown rot of wood 
Contopus ({Class Aves] Passeriformes: Tyrannidae) 


borealis Swainson... 65. PsP SR Res Sd Red RG, Ste 536 

sordidulus SclateP? 2.3. 00 6a. nn a Ae SEL, Se A, ee hee 536 
Contortylenchus ({Class Secernentia] Tylenchida: Allantonematidae) 

brevicomi (Massey) Rithimic i. p26 wae oon. DD A OS, ieee no 408 

elongatus (Massey) Nickle: /. ce) SS eee 6 age ses a aw nn UR 404 

reversius (Thorne) \Rithin 2s: paee tes cea oath ce au OW RRR ne ee Pe ee 404, 536 

SPP. Nara Gi, aie A eis TRI ia ATR CIR G Soctio a) Eh weir ee 405, 408 
convergent lady beetle; Hippodamia convergens 2g) ica cs on cn son: ss ane ae eee een 129 
Convolvulus arvensis L. (Solanales: Convolvulaceae), see field bindweed 
copepod, \([Class’ Crustacea] ei coc its A ayin te: ore «nite et cee Sens ee ae ee 71, 159, 284, 295 
Copidosoma (Hymenoptera: Encyrtidae) 

bakeri (Howard) oy e4 3 1S eck ene. SATIS ert 317 

fruncatellum (Dalman) 825282 2. Nn Sine yo hoes AES we claire etd Uda ena 30 
COMMS ZEG ING See seals eats ae tc oe 30, 62, 71, 97, 124, 159, 288, 289, 291, 305, 315-318, 323 
corm 


earworn/bollworm/tomato fruitworm, Helicoverpa zea (see also nuclear polyhedrosis virus [NPV], 
and singly-embedded nuclear polyhedrosis virus [SNPV]) .... 17, 26, 35, 36, 62, 65, 68, 70, 71, 279, 
280, 288, 289, 301, 302, 308, 310, 311, 318 
rootworms, Diabrotica spp: (see also preparimes) in 5 acvestears ese ones ot me eee 51; 54,57; 67; 68,71; 317 
Stunt-spiroplasma,; Spiropl asia Kurakelligng cao tiene) nos citer eve reee-ed croc egg oe 305 
Corticeus (Coleoptera: Tenebrionidae) 


pParallelus'(Melsenleimier) s+. ssn cent a aosicie ote’ deere uate etielin ha oe tk a oe 535 
Substriatus:(LeConte):  .i47'a.aig na df cows tgdns # ese eS An asa ais 5 aS Sie 535 
Coritciunt: [Class Basidiomycetes |. sccean.c sctamdtats et sted. Sins ate aee ce te ee Se 
Corvidae ([Class:Aves] Passeriformes): (c.:2.5- cca evn tew su, vis, ove sececoete item hen RR RRRRee ema arene tno ana 536 
Cotesia (Hymenoptera: Braconidae) 
flavipes (Cameron yyy oo vieie o stle ay bo = Wistiel op Ore ad 65 ela Be) we I le PGP 128 
glomeratus (Linnaeus) 12252 See once s cits laile\w «vie ahaa MO RE. A 3, 6 
marginiventris (CTeESSOM) few dota. Wee as apie = Raw As 04 ale wis chs a eee ere aes ee, 65 
melanoscela. A AEN. Ee ROE anole targoudare te yh G ainsi LR EEO arn ant 417 
Wieldnmasee) s+ (Ratze burg). han nana tata thie arte home cake ee 103, 111, 417, 419, 420, 422, 423, 430 
rubectla (Marshall). 433 «i 4 sg SSSA AE eek a Cee 31532 
SPP a Lees Sale Bi wa Hh RR ae EEN iaaree te las Nip RU 29 


cotton, Gossypium spp. .. 29-33, 57, 62, 63, 69, 70, 96, 123, 124, 130, 271, 272, 279, 282, 318, 319, 321, 413 


* Editor's (JRC) Note: When the species Apanteles melanoscelus was placed in the genus Cotesia by Mason 
(1981), there was some confusion among biological control authors as to the proper gender ending for the 
specific epithet, and the species is given as Cotesia melanoscela in some subsequent publications. However, 
according to R.W. Carlson, ARS Systematic Entomology Laboratory, Beltsville, MD (personal communication), 
Cotesia melanoscelus is grammatically correct, as is also indicated in Mason's paper. 


598 


cotton 


De HOLCLOUST Cals CO Lermmr nT Mh UMPIRE NT Rete cel) rice y's ik eso etek Oe ed RON APL EE a 29 
see een ane Ser be nner eer, Met NOY fad ba eed a kale d add aad annwles en 271,202,282 
Fea Perroratory DUCcculGINLe L/UEOET ICH Caan jot as oot el es cles dy BO 29, 36, 270-272 
IeAIWOUIN Me ALODUIM DE GL CILICEORIN a ee ener ais ceed eae rs ceca eb ee SRR DY 17, 318 
FeO IMOpielOlsmests:0 laments wr Nin GA NOS Pty paw TEP aes a POO es AG 292305917 
SOUCHI WORM ZOT IT MIGCHOIGES ORE E OER RE em rach heart Stree tee ee ee ER 104, 414 
COUOMWOOU SAN DEELIO IC /VSOMelASCHIDIGiNMn fo 2 ON Seba vee lage etre the ds 104, 110, 414, 428 
COL CUSHION SCALE MICEIV 2 DUlCHNaSiva etna ee oe ie Awa bee les abe de sch eee) 550292161 
CPV, see cytoplasmic polyhedrosis viruses 
Cla DIsC ICTS el ONIISIdAC Mer an awn en MMS are ms SP he ek a CM OO ie eR 412 
SEAUOCthy er MECH ME SDI Maram acre maT Mee ees ees ae etek eee SMES UP en MIE ee, 99 
Cremifania nizroceliulata’Czerny (Diptera: Chamaemynidae) 2c. 2. ee 454, 539 
CTOOSOLEUUISHLUIRCUNIT TCCTIEAIGML ATs Me amntene eter hn Gta eee ee en Oe let ey ere 77, 81, 82 
SU Ket Cr Vil ac ermeenn er eevee ae Mae Hn fe Sere GORE Tea eon aa less eee a eae oes baa: 512 


Crioceris (Coleoptera: Chrysomelidae) 
asparagi (L.), see asparagus beetle 
duodecimpunctata (L.), spotted asparagus beetle, see beetles, asparagus 
spp., see beetles, asparagus 
PCOMATENIT StS Mer OMALITUNT SDD Fea rT tr eh eale ore bhi oles elated ea Reale wba e als 456 
Cronartium ({Class Basidiomycetes] Uredinales) 
quercuum (Berk.) Miyabe ex Shirai f. sp. fusiforme, see fusiform rust 
ribicola J.C. Fisch. ex Rabenh., see white pine blister rust 
spp., see Cronartium rusts 
crotalaria, showy, see showy crotalaria 
Crotalaria spectabilis Roth (Fabales: Fabaceae), see showy crotalaria 


CEE AEA OT DUCE TUNE (DRIC/ACICRSMRE OM Poste hee ek coke he se tees betes cae se lie 90, 95 
Cryphonectria parasitica (Murr.) Barr ([Class Pyrenomycetes] Diaporthales), see chestnut blight 
ty Denar eRCe Mee ane mar Curr pr ra LING CUO Gs as ukiw tiles phic dk Ang pleas Eek we os 456 
Cryptaphelenchus latus (Thorne) Rithm ([Class Secernentia] Tylenchida: Aphelenchidae) ............. 536 
Cryptococcus fagisuga Lindinger (Homoptera: Eriococcidae), see beech scale 
ayn oi cemisnc oleopictay COCCINE | NdAe)— te ean. 5. Da. ee he tans renee ae Melee e ethno. as 10 
Cretan allo Vavitlicae® Mere imie gs hehe eres 8 So. Wala MA Se PRE L ER AG Whee heehee e ee et 2os,542 
Ol wostanedmrassnOpOcleerare een at abe the nL etry. a oe eG ee eee be ees ee ee 312 
Ctenocephalides felis (Bouché) (Siphonaptera: Pulicidae), see cat flea 
Ctenopharyngodon idella Val. ([Class Pisces] Ostariophysi: Cyprinidae), see white amur 
MCHC ACH OOLCODClA i emma ren tn cletme ss whit web wate Stable eee le te ce eae Se ca Saas 535 
Cucujus clavipes var. puniceus Mannerheim (Coleoptera: Cucujidae) ........... 0.0... cece ee eee 530 
Ue DEER GNCHPIIS SQUVUS AEE aR MEL LER Le hG Sae eee eR Ont he es eee eee ae ates sb dee bs 67, 93 
Cucumis sativus L. (Violales: Cucurbitaceae), see cucumber 
Cucurbita spp. (Violales: Cucurbitaceae), see squash 
Culex (Diptera: Culicidae) 
pipiens fatigans Wiedemann (= Culex quinquefasciatus Say), see southern house mosquito 
quinquefasciatus Say, see southern house mosquito 
POS UATISE DEO AIMEE Te kc sice tins d ca Rees eee A ee a eet OME Sak eed 295 
RGU Ori ear ICL Metta HNN oS esd Ge eT eke T RR eee ee ss Mt eho uies case ob 281 
AES ae OL Ct ee ee eR OMe RL er te et ets Deine site als cede tees esa ns 281 
Culicidae (Diptera), see mosquitoes 
Culicoides cavaticus Wirth & Jones (Diptera: Ceratapogonidae) (see also non-occluded 
MSO | ee rn es Me eon ee Pe ee hE re es ke a wen ee ele as 69, 281 
Culicosporella lunata (Hazard & Savage) (Microsporida, Caudosporidae) ................00+.000ee. 295 
Cupressus (Pinales: Cupressaceae) 
Itty titre) AWE PS. cate Ale 9 5 A OPE oaclg wrath ch eile Ne gr ira ar ee 111, 416 
spp., see cypress 
ETIEELOCMEE IItET CLISDUS MAIER NE CRE (oii note Sls Vibe eh cs Se. Wee eam oe SE eee teense es 76, 81, 87 
Elly itis PenidO tera wm MOCTsICME Wen tenets ales e's eels srs nee he wat oes ctl e ee eles epee al 
Cybocephalus sp. prob. nipponicus Endrédy-Y ounga (Coleoptera: Nitidulidae) ........... 59, 124, 125, 140 


okey 


Cydia (Lepidoptera: Tortricidae) 
pomonella (Linnaeus), see codling moth 


SPD: fb fascehrild Bea ble vi eee uate sigh e Osco iy os «aoe © Sacer wg ieee ere 102 
Cylas formicarius elegantulus (Summers) (Coleoptera: Curculionidae), see sweetpotato weevil 
Cylindrocarpon gillii (D.E: Ellis) J.-A» Muir (Class: Hyphomycetes] |... 4. . decqastemiees ene eee ree 466 
Cylindrocladium [Class Hyphomycetes]| scvn oes oven en oe soe es = ee ee eee 459 


Cynara scolymus L. (Asterales: Asteraceae), see artichoke 
Cyperus rotundus L. (Cyperales: Cyperaceae), see purple nutsedge 


Cyphocleonus achates (Fabraeus) (Coleoptera: Curculionidae) . ....... «as gent. sya a eee 85, 140 
Cypress; CupressusiSPP.: Ce «Ges a cers © x yen al etuOTe eo Mena = (Sng cS upto at aa ici ca 455 
’eypress aphid," Cinaracupressi x once sta ohio ae aise tun ee, wee ee a 107, 454, 455 
eypressispurge, Euphorbia eyparissias oy. 4.50 alae «es se ee 79 
Cystiphora schmidti (Ruebsaamen) (Diptera; Cecidomyiidae),.2...4.)-..capyaiie seer ary ae ee 84 
Cytisus scoparius (L.) Link (Fabales: Fabaceae), see Scotch broom 
cytoplasmic:polyhedrosis viruses (CPV) (Réoviridac) 2.° 2.70... 2.. 22 ee 355 2/2, 282, 31954353 
of:cabbage looper’; 25.0 ech sale a8 fc Se Mian pads aos vee Sane tad nce ee 35,282 
of Douglas-fir tussock moth i042. dhwtad G2 eso visred eo. gine ahi eee ae 435 
of:pink.bollworm2 Paid 5 « .\Uagiagvea nd eed wom < bdlaod attire eee, 2. eee 70, 272, 300, 319 
of tobacco bud Worm ace lassi uty sae. Rites Fake Wl oe “ees es cuus eae 9s Che age ioe 319 
D 


Dacus (Diptera: Tephritidae) 

cucurbitae Coquillet, see melon fly 

dorsalis Hendel, see oriental fruit fly 
Daedalea berkeleyi, = Gloeophyllum mexicanum 


Dahlbominus fuscipennis (Zetterstedt) (Hymenoptera: Eulophidae) .....................05. 114,11 5e0te 

Daktulosphaira vitifoliae (Fitch) (Homoptera: Phylloxeridae), see grape phylloxera 

Dalmatian: toadflax;.Linaria.dalmaticads wycnn® tecture aoe ee ee ne ee 36, 37, 76, 78, 79 

damping-off 
of cotton, Rhizoctonia solaniand Pythium ulomum eer ae ee 96 
of ornamental plants, Rhizoctonia:and Pythium sppas see see eo ae ee eee 94 
of pine seedlings, Pythium debaryanum >. ....).....+,0. 2c--4 =. Sa eee 13 
Of pines nu Sey aatss oes aa Uae See ean cue © Sao were x Gur paar outa eee ee 118 
of rediand. white pine.seedlings. /usariumsppo 2... os oa ee... ee eee 456 
of vegetablesy Rhizoctonia and Pythiumisppx ae entaaeerl: see oe ee 94 

dark-eyed junco).Junco,hyemal isin (cx: Sune Wn aoe denne oe ea ane cece tetiy sent 434 

darkwinged fungus gnats (Sciaridae) =. sehen oe «ness tes onin eee a eee 0) ee a9 


Darluca filum, = Sphaerellopsis filum 


Dasineura'spnr. capsulae Kieffer (Diptera: Cecidomyiidaé) . 22... 4)... oe ae 85, 141 
Datura stramonium L. (Solanales: Solanaceae), see jimsonweed 
Delia antiqua (Meigen) (Diptera: Anthomyiidae), see onion maggot 
Dendroctonus (Coleoptera: Scolytidae) 
adjunctus Blandford, see roundheaded pine beetle 
frontalis Zimmermann, see southern pine beetle 
micans Kugelann, see European spruce beetle 
ponderosae Hopkins, see mountain pine beetle 
pseudotsugae Hopkins, see Douglas-fir beetle 
rufipennis Kirby, see spruce beetle 
SPP. ais dia wre aves BERS n wee idieen Ricp Spe ol ona Skah tele 2a oy ek eae ce rare ea el ee 402, 403, 409 
terebrans Olivier, see black turpentine beetle 
Dendroica coronata (Linnaeus) ([Class Aves] Passeriformes: Emberizidae) ......................... 536 
Dendrolaelaps sp. ({Subclass Acari] Parasitiformes: Digamasellidae) ................0 0c cece eeeeee 409 
Dendrolimus spp. (Lepidoptera: Lasiocampidae), see "pine caterpillars" 
Dendrosotor protuberans (Nees) (Hymenoptera: Braconidae) ...............0ccc cece cues 109, 401, 402 


Derodontidae/derodontid (Coleoptera) 3 732-2... he en ee ee 453, 537-539 
Deuteromycotina [Kingdom Fungi] 77> 2.45 2 ee 314 


600 


Diabrotica (Coleoptera: Chrysomelidae) 
balteata LeConte, see banded cucumber beetle 
barberi Smith & Lawrence, see northern corn rootworm 
virgifera virgifera LeConte, see western corn rootworm 
SpOstsce aisd Colm TOOEworins alld peetiess CUCUMDEr)* 2a ce era e ee bees boa ae dea ee ves 54, 68, 316 
HAGECIM DRE Tara Wviaiiel Nei Mer ee ees Se OE se all baa a ee eb ee ead ee eee de 303 
howardi Barber, see southern corn rootworm and/or spotted cucumber beetle 
Diachasmimorpha (Hymenoptera: Braconidae) 


PEACICOUGGIG CASHINGAG Maye a net een et Metcie ee AS lars See ava a wk ee RE SY 63, 66, 129 
TEV ORT AINGT ON) anette we aI Pee i cr cage incre he Pe EEE Ges OE ee 63 
Diadegma laricinellum (Strobl) (Hymenoptera: Ichnuemonidae)........... 0.0... cece eee eee 440-443 
Dialeurodes citri (Ashmead) (Homoptera: Aleyrodidae), see citrus whitefly 
damondbackimot r/iwellaxylostellay s\n es Pale. ers wes Oe 81936; 7152709292. 3095310 
Diaparsis temporalis Horstmann (Hymenoptera: Ichneumonidae) ............... 00000 cece cece eee 140 
Diaphania nitidalis (Stoll) (Lepidoptera: Pyralidae), see pickleworm 
Diaprepes abbreviatus (L.) (Coleoptera: Curculionidae), see also citrus "root weevil complex"........... 68 


Diaretiella rapae (M'Intosh) (Hymenoptera: Braconidae: Aphidiinae) 
Diaspididae (Homoptera), see scales, armored 

Diatraea saccharalis (Fabricius) (Lepidoptera: Pyralidae), see sugarcane borer 

Librachoides dynastes (Forster) (Hymenopteray Pteromalidae)t. va. cs Paes. ce EO ee eae, 138 


eucnropius esonvaius Gigiio- Tos (OrthopteraAcrididac) iv. .sc0.\ce8 tal OV Oe PPR a ee. 313 
Dicladocerus (Hymenoptera: Eulophidae) 
ELON ISRY OSIIMIMOLO tres. Caer es Me Moy, es ie Soler edn ane, Oe wha a Pe eee bee ee ee 442, 443 
WCSEVPOUGIELW ESEWOOC ME ee eee are Eee ee ae oe rele ear OM See. 440, 442, 443 
Minreremiian el aaSHhOUDeI VICICTOPlUs dIffereniiqus. vss ty. sa 2h as. eeRE Lid See Hue eC ba ee eee 313 
Giiise Knap WeeGr CEMAUed AIfUsA* ToS ae oe he RSs soe ob. Oe ee Bee 76, 78, 79, 84, 85, 90, 123, 140 
Dinotiscus (Hymenoptera: Pteromalidae) 
CLTAS CPLOV ATCC eee net ets tenets a) Ped 2 Pe Sob leet Mee eho? AS TOT a 2 TS 3978535 
PAIR CUUCTOWILOLG) Mee aa en a ne ee ee oe aaa s COU soe bel Veet ee oes 535 
BETATOCIONN  ASlINCAG) wreak ihc Gr are he ee OL Me Ae re oe es ens aula SEPA is 397,335 
328 jaacs os egue shesalatoltigk Me hol okt Sickel oe a OE aC ae ee ee EO ee a ee a ee ee 397 
Diospyros spp. (Ebenales: Ebenaceae), see persimmon 
Pipigpastesiiae (( Class occemenlia) KNaDdtida) > sn. kies aes 5 Sew ARO TE tS See ha clam 405, 536 
Dipriocampe diprioni (Fermiere) (Hymenoptera? Tetracampidae) . .. 2. 256 ieee cde e edit e cece e ees 114 
Diprion (Hymenoptera: Diprionidae) 
er ee a ed rmed rien nen nqee Ses Dhaest, PL MII, 417 
similis (Hartig), see introduced pine sawfly 
Diptera/dipteran/dipterous, see.also flies’ js ewicas docs css cer eesee ews s 280, 300, 322, 396, 397, 401, 413 
DlCOd SUCK IND men eet ee aon a aca! he cee yet fae EAs eu awa as de oeere LTS. ASS 280 
Ditylenchus phyllobius (Thorne) Filipjev ({Class Secernentia] Tylenchida: Anguinidae) ....... 123, 128, 141 
Diuraphis noxia (Mordvilko) (Homoptera: Aphididae), see Russian wheat aphid 
Wolenopouidac dolichopodid (Diptera)yonwe, meres: fob 26d. es cree FLEA eG ts 397, 398, 535 
Douglas-fir) Pseudotsuga menziesii ......6.2...0550: 117, 396, 433, 434, 436, 437, 449, 451, 460-462, 465 
Douglas-fir 
beetle, Dendroctonus pseudotsugae .... 01. ccc ees 101, 102, 108, 396, 403, 405, 409 
Pole Dee meme DSCUCONVICSIIUS MEDULOSUSUE? Mae. ee eee aI Te ee os ses ies spate ss ee ees as 408 
tussock moth, Orgyia pseudotsugata (see also nuclear polyhedrosis virus [NPV])...... 101-104, 107, 113 
428, 433, 435-438, 443 
downy 
PHONY OFT SEC GION UPR PIT WR rr vec lole Machen y cia ae Seats Weeds KOT ela ED eee De) Need Se 90 
MODUDSCKel MT 1201 0eS DUDESCENS Geers tween aa chs 1% GA Rea eee Taw EA Lee ee eee 396, 397, 536 
Drosophila (Diptera: Drosophilidae) (see also'spiroplasmas) 2.2.20. .s sete ee eect ee 305 
Drosophila sex ratio spiroplasma, ([Class Mollicutes] Mycoplasmatales: Spiroplasmataceae) ........... 303 


Dryocopus pileatus (Linnaeus) ([Class Aves] Piciformes: Picidae), see pileated woodpecker 

Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae), see "oriental chestnut gall wasp" 

Duboscqia penetrans Thorne 1940, see Pasteuria penetrans 

Dutch elm disease, Ophiostoma ulmi... te ce eee ee ene tee eee eens 105, 118, 401, 457 


601 


dwarf mistletoes, Arceuthobium spp. . odes ¢ Jn oe ea sans sas» oo eee ae 102, 119, 465, 466 
Dysmicoccus (Homoptera: Pseudococcidae) 

boninsis (Kuwana), see gray sugarcane mealybug 

brevipes (Cockerell), see pineapple mealybug 


E 
eastern 
cottonwood, see cottonwood 
white pine, see white pine 
"eastern spruce budworm," see spruce budworm 


Edhazardia aedis (Kudo 1930) (Microsporida: Amblyosporidae) ............. 00sec eee ener eee 284, 285 
Edovum puttleri Grissell (Hymenoptera: Eulophidae) ...................0esaee 57, 60, 61, 128, 139, 146 
egeplant, Solanum melongenarws iu sine ca Re Etro «4 eae me eee heey ee 60, 61, 94 
Epyptian alfalfa. weevil; Hypera! brunnipennis tact van oe ail a eee ots ee eee eee 25 


Eichhornia crassipes (Mart.) Solms (Liliales: Pontederiaceae), see waterhyacinth 
Ektaphelenchus ([Class Secernentia] Tylenchida: Aphelenchidae) 


obtusus Massey io ssov/eaied ean o,30s, 4.0 5 nteholats bikes BRE daandaee agente egiaaeia + - Gleam 404 
fenuidéens: (THOME). 5 ence. cs ea cusiayes om nelg A oie wm eoeuns on)» obo ene, eM eg ait Sen cee seen 536 
Elachertus argissa (Walker) (Hymenoptera: Eulophidae) 75s, 0) < rus ae carerne ts «iets eee 442, 443 
Elaeagnus angustifolia L. (Proteales: Eleagnaceae), see Russian-olive 
Elateridae (Coleoptera), see-also wireworms . ....... ...<tsot sein enter iy eee > oe 67 
elm, 


American, see American elm 
Siberian, see Siberian elm 


elm 
leaf. beetles Xanthogallerucalutéolay, faci. b gece ee ae 7, 15, 16, 18, 24, 25, 54, 414 
spanworm, Ennomios:Subsignaria ini o. 5c 5 iu |} ela cee y, Behe ee ne A) oe oe ee 102, 110, 415 
Emberizidae({ Glass Aves];Passeriformes), .., ..2 5 42 sm 2 sare aie ie een pc) ee 536 
Empidonax:sp. ([Class Aves] Passeriformes: Tyrannidae) 3... .2 4.52) oo a eee 536 
Empoasca (Homoptera: Cicadellidae), see leafhoppers, Empoasca 
fabae (Harris), see potato leafhopper 
vitis: (GOthE) (s.s4 5 Psusiinctun ee eee Aedes digo os. ie, 42 eaten rage meeus  Dok nadie OI ed ae acl 330 
Encarsia (Hymenoptera: Aphelinidae) 
clypealis: (Silvestri) i... is: «4% age. F yoed Re aS hee F aciaew nent ay aes Oe pene 127 
Sormosa: Gahan sixes otahis Bh Fay Ree ene ate vbw snes de Shige « aaa ame eee neg wee 137 
Jahorensis (HOWatd x Gaeee sai c.c escola icdack ote ev eee Ok ae ee 123,328, 37 
dutea (Masi) 0g: aerate ee yk Peo ae is orate ead ago sa eed oe, ocd oN Ee A ea IN eee ieee 137 
nigricephala: DOZIer epee awh 6 6 5'= +, eld iw 20 DS Sings. e oa ec ee 137 
opulenta (Silvestri), Sa: se Rae ee ot tee Reka ss ee Pccleeeen ee ence a a 127 
pergandiella Howard sxe scious daiategeah vin Mow Seay ake Ae ob onda eee © ee wee 137 
smithi (SiWvestt) cas ok iauphanhieeenia hae caps Sa titer stn heel ce ee 127 
sp. nradiaspidicola( Silvestri) Geieey. oak oh 4 ede 2h he Ces oe ee 140 
sp..nrasireriua. (Silvestri) 2G: aie tcciiet fie Pee Bie: cies toc = sans. crcl a See ec 137 
SPDs a aks 7, gappiocitthhonts, aes “eee dee 0 5 See eee et er sence tee a 125,437 
iransyena fahimberlake):setne¥ aceigers DORs. sso ones casa ae > SR a ee ee 137 
Endogonaceae ([Class Zygomycetes] Endogonales), see fungi, endomycorrhizal 
Engelmann'spruce weevilissodes sirobi Aare seein ties eee Sane ee eee ee ee 101, 396 
English grain aphid; Sitobion avenae (see also grain aphids)... ....2-4..<.+-0ccescrsr ou esusseueen 161 
Ennomos subsignaria (Hiibner) (Lepidoptera: Geometridae), see elm spanworm 
Enoclerus (Coleoptera: Cleridae) 
lecontel (Wolcott) tuneoanan dS Sie AAs} eal Se ee See ee Be) 
sphegeus (Fabricius) ives, wie Suis) disaracidels :ereaailals mp Nites: aif mc oa eee een 398, 399,535 
Entedon leucogramma (Ratzeburg) (Hymenoptera: Eulophidae) .............. 0... 0cc cece e cece eas 402 


Enterobacter cloacae (Jordon) 1890) Hormaeche and Edwards 1960 (Gracilicutes: Enterobacteriaceae) . 96, 99 
Enterobacteriaceae [Class Bacteria, Gram-negative facultatively anaerobic rods] ..................... 273 


602 


Entomophaga ([Class Zygomycetes] Entomophthorales: Entomophthoraceae) ................0.0.000 i 
Pe ERETESERING) DAtKOnLOG4 "ery eine HermrCo en ak WEs AN CHU IE Me Wes vd TA, 312, 314 
maimaiga Humber, Shimazu & Soper in Soper, Shimazyu, Humber, Ramos & Hajek ........ 115-72;,106, 


112, 158, 314, 315 
Entomophthora ({Class Zygomycetes] Entomophthorales: Entomophthoraceae) 
coronata (Constantin) Kevorkian, = Conidiobolus coronatus 
grylli, see Entomophaga grylli 


Patomoonuor ales entomopntnoralean tse me ear ee ve deed dhe ndwa dae v8 AY weed awe 3149315,330, 331 
Eoreuma loftini (Dyar) (Lepidoptera: Pyralidae), see Mexican rice borer 

Ephedrus plagiator (Nees) (Hymenoptera: Braconidae: Aphidiinae) .............. 00.000 cece eee ee 138 
Ephestia elutella (Hiibner) (Lepidoptera: Pyralidae), see tobacco moth 

Prmaitesoriario (Cresson) (Hymenoptera Ichneumonidae), «<< iadse4 2 ace w Adee. oo SO 445 


Epilachna varivestis Mulsant (Coleoptera: Coccinellidae), see Mexican bean beetle 
Epitrix hirtipennis (Melsheimer) (Coleoptera: Chrysomelidae), see tobacco flea beetle 


Ppureaunearis Naakilll (Coleoperas NiMMOULICAe) "<P ilscs oo 28s o.oo RII Pek By Ras J OIE 53D 
Eretmocerus (Hymenoptera: Aphelinidae) 
PLA SCLC CL men en ee eae Mice Waser rpm eens): | ian 5 44h GL ain! < Wie ah eam a CR eee ANG 137 
SO es ee Rs nea Help gw eins OSA. be oa ae ROO RNR & 1258137 
Eriborus terebrans (Gravenhorst) (Hymenoptera: Ichneumonidae) .......... 0.0.0.0 cece eee eee 124, 139 
Eriophyes chondrillae (Canestrini) ({Subclass Acari] Acariformes: Eriophyidae) ...................... 84 
Ponopmconnerd Villisant( Golopteta ,Coccinellidae iy i. 2. asia a a ouve oe. nao) eee IU oes 137 


Eriosoma lanigerum (Hausmann) (Homoptera: Aphididae), see woolly apple aphid 
Erwinia amylovora (Burrill 1882) Winslow, Broadhurst, Buchanan, Krumwiede, Rogers & Smith 

1920 ([Class Bacteria, Gram-negative facultatively anaerobic rods] Enterobacteriaceae), see fire blight 
Erythraeidae, (Parasitiformes) 
Escherichia coli (Migula 1895) Castellani & Chalmers 1919 ({Class Bacteria] Enterobacteriaceae) ... 72,324 
Estigmene acrea (Drury) (Lepidoptera: Arctiidae), see saltmarsh caterpillar 
Etiella zinckenella (Treitschke) (Lepidoptera: Pyralidae), see limabean pod borer 
Eucallipterus tiliae (Linnaeus) (Homoptera: Aphididae), see "linden aphid" 


EP eee OtOpia cra a ACHINOAG eeu tnian Me ten Be cee ea eke Mee in Ry OY Tees ot 31965 
PIUAHE SADC OSKY Uae ete end RED ie ARE eS Wee 2 THE es PE RE SLI lie ah 65 
SUD ee ene een te ee Le chal, Sales a ln wlaiois Sip hie Reais arb evayaile a Mea Pe ey Paiste hoes oe, By 66 


Eugamasus lyriformis, = Schizosthetus lyriformis 


eumenine wasps (Hymenoptera: Vespidae, subfamily Eumeninae) ............. 00... ee eee eee 448, 449 
evonymius, Luonymus spp: (Celastrales: Celastraceae)o 25.0: we. dud Ss Es 124,°1257130 
SHONYMUS SCALE "CO MGSPIS 'CHONMVINI. . eka cede sea eh wee en 42, 51, 54-56, 58, 59, 124, 125, 130, 140, 162 
Bane lanoae cape mid s) 1 Hymenoptera inti aane olen yo ates fe ee ee SP, 419 
PpemaemniGad le Iptcraxoyipildad). 2 .cvswam ha hhnean soe. Six cet tesnee rie hee UEP... 138 


Euphorbia (Euphorbiales: Euphorbiaceae) 
cyparissias L., see cypress spurge 
esula L., see leafy spurge 
pulcherrima Willd. ex Klotzsch, see poinsettia 
spp., see spurges 
Muplectus pert Gordu (Hymenoptera. Pulopnidac) tenes .. ee ess. Ve sols se ees Soe, 1, a Y 
Euproctis chrysorrhoea (Linnaeus) (Lepidoptera: Lymantriidae), see browntail moth 
Eurasian 


PING BUC CMRINEL SULT ee N, e e s ima e May sea eee a ess 54, 58, 59, 161 
DOL idioms ise aM OSOr a LAICIMIDODUITIA Gi tes fi haa a Wingo Sa ee ee a ee ne 107 
Ry AterinI OU IOV LIN SDICOUIN: Hak on nen A Raat usr tenets ins Peel 39, 76, 79, 80 
European 

PU AOP MT ZOU OO USING) IIS eae arin Ln ears y oie RVG «tines GANS Los Ss SSA PTS 4 18, 24 
corn borer (ECB), Ostrinia nubilalis .. 8,9, 11, 15, 16, 18, 26, 34, 35, 54, 56, 72, 124, 139, 158, 159, 291 
CAE OL ICH OU ICHICNIA Bee Re Nee CC tan oN Ce a Ress RP OR MERWE EWN T Pa ems S29; 15 
elm bark beetle, see smaller European elm bark beetle 
SNSCAle MOSS) DUG SPUliCie neon PAR ean Ree aR ck ook CPaws Cees eS Yee, CR el. 18 
foulbrood (EFB) disease, Melissococcus pluton (= Streptococcus pluton), see also 

LOUD COOGEE AEA Ie MR ye Faron er eee ek Cn re hah Me Weide e hewn Sawin 274, 296-298, 328 


603 


larch, see western larch 


pine sawfly, Neodiprion sertifer (see also nuclear polyhedrosis virus [NPV]) ............. 102, 104, 438 
pine shoot moth; Rhyacioniaibuoliana Wes ene. ioe a ee 8, 15, 24, 101, 102, 110, 410, 411 
spruce’ beetle; DeridroctonusynicansiG iran foci su u ies ok se 6 ohio oe eo orem ne ent ee 395 
spruce sawfly, Gilpinia herqyniae gree eee. ois Enea pelea Rey aoa eee 16, 105 
wheat stem sawfly, Cephus pygmideus . .. dian: eal. ets ie Fh ee ee eee 16, 18, 56, 161 
Eurytoma (Hymenoptera: Eurytomidae) 
Cheri Ashmead 63 206 Pain. oo eS oe Winnie pines we clam Gore 9S ee 335 
SP): GE. BUTE OR BRS os ie os ORR Se S.A eo ea ee ee 141, 399 
Eurytomidae (Hymenoptera) ® 20s) 2 SSeS A ey cece rn ee 535 
Eustenopus villosus (Boheman) (Coleopteras Curculionidae). 0 \. 9 ete ste ce eee 84 
Eutrapela‘clemataria GE Smith) Go ke eee siete ike eos. SR nes eee 415, 416 
Euxoa auxiliaris (Grote) (Lepidoptera: Noctuidae), see army cutworm 
Exenterus amictorius (Panzer) (Hymenoptera: Ichneumonidae) ....................24 000s Li4 Isai 
Exochomus (Coleoptera: Coccinellidae) 
lituratussGorbharm os isle. RBs 2 Se Gee oe Oe steel. pbc, PINE oe, 539 
uropygialus; MUSANt iy cis cans Spud vise ol Oar Sa oo bi cue e « qo eee el ener ee se 539 
Exorista (Diptera: Tachinidae) 
japonica (Townsend) > ac. BA Rae eh ok ak eT eee 421 
rossica Mesnil x2 2... 52s Pa se Pa a Fe 421 
extracellular:virus(es)\(EGV.) Steere oe oe ad ters si a = eR ctr ee eee de 301, 302, 310 
F 
Fabaceae (Fabales), see legume/leguminous crops 
face fly, Musca autumnalis Soca ne tee < Soc + +e a oe ee eee 24, 25, 28, 33, 64 
fall 
armyworm, Spodoptera frugiperda (see also multiply-occluded nuclear polyhedrosis virus [MNPV], 
nuclear polyhedrosis virus [NPV], and granulosis virus [GV]) ........... L7S3Sp TIP PS8p283RZe9- 
301, 303, 304 
cankerworm, Alsophila pometariae® DRE pew, A ee ka so |. 4: « ee 111, 415, 416 


Fenusa pusilla (Lepeletier) (Hymenoptera: Tenthridinidae), see birch leafminer 
Ficus spp. (Urticales: Moraceae), see fig 


field bindweeds@ommolvulussarvensis 42.42. s1824 a0, oe ee ee ee 76, 82, 83, 86 
fig, Ricus: Spp tere 5k 035 a wae aid wean ox SSRN Me Ec 68, 278 
fig scale; Lepidosaphes conchiformis 3.25 <u 8.cn wes 2 eR el a A ee a 18 
filamentous virus:(ofihoney bee) 2jut. $4 sso easy eeu en ats dele <> ave bo ea 298 
Filipjevimermis leipsandra Poinar & Welch 1968 ([Class Adenophorea] Enoplida: 

Mermithidae) ts... 4.2.0 2s 36 2 bbs nb ere etasonen oncces ERE ae eee 33, 3169307 
fir(s);sAbies: spp, (see:also Douglas-fir) aay ae eres 115, 412, 413, 433-435, 444, 447-479, 453, 454 


alpine, see subalpine 

balsam, see balsam fir 

European silver, see European silver fir 
Fraser, see Fraser fir 

grand, see grand fir 

lowland, see grand fir 

Pacific silver, see Pacific silver fir 
silver, see silver fir 

subalpine, see subalpine fir 


fir engravers Scolytus: ventralis (26 sees. tae a ele Se be ee ee ee 405, 409 
fire 
ants Solenopsis:Seminala <= lossl acne Se eee Ieee 35, 54, 67-70, 158, 159 
ants, see ants, fire 
blight; Erwinia:amylovoras’ i 205 2a TARR ss sie eo 93799 
"firetree," Myrica Jaya sios'5.2 co SER a eR RO ee ee eee ee 466 
fish [Class Pisces] (0:05 cata utp bie Sale eed Bae Re ie ee ie a 436 
flies. (Diptera): ..1\...... . joke Bain Serie eee ee 25:69), T2pS97305, 322 
AQUATIC” Sua pies vias: suis. hse ole leis w POS BUR are bite NG SR SU Rene cr Pele] 


604 


TBM (ORNS RIE 0. aj own oly © Oye One Dak Caen 400 
Sis Rr eee a 2 eee Ravel dnp nS ea aly ie we Flap Mageh aelewapenee a diy 254, 3210322 
CC STHENTNTG RO) 0 a ee ee ee 71, 159, 284 
Bae Deere an) ae I aoe is ep ant et aed + rope teforagewss nf apa dae vein (sparen oan 4 280 
erate ihe a IE rN eet ies is 9 nd © 3 fa acl « > os qRaybrfimodnisagyvaie Aas ara.a ws acnay’yaceni'’. a 54, 58 
UCASE TTC SEAN ys uate knit are REP rE USP 5 Gita 7 ea palde Layrrierrand aos Buel E @ # aye sm anegs wiv enue hans 342 
SN ne ABLE GA DOR a te Sane 6 2 Ooo i.e ce rr 329; 330 
RRO MCGEE COD DAL ECIIG:) ar Wes ere EMRE RUN NAG BG ook ca 44d inn don dyPle me denser 4.030 eemvecann 36, 308 
COIL RS ote WOT) © CEMENT aemseeed ce tn ea re ae 8, 16-18, 26, 63, 68, 84, 86, 267, 278 
horn, see horn fly 
BUGS Nich CATV) apatite mtd oe NIE tive Pi ee 2. ats Suc Sorys uaiiG Deed ioe WR, wicsnjangy le, Wid ALS bd, 9,0 lb a anes ocd 4 305 
house, see house fly 
Fearne OCOD ZICAC Nee tere Sew Pee em Fhe Re al Ie ee Ne aan Hell Gui bheh hg odes 26 
ACESS Fe WA AIOE 2 9 ize Seed ene icine ai ee, A a Pl LD, 322 
Ri reeetn Ch oteted aint MINGUS OCC) esta tm teeter ens ei ued AUN Sx. haces a, 2,9 v4 apm caasih Mw fe raln dM mcadal le wb Aotogp 64 
TRUE Stee COC) am PN ee I EE eG lh pols <_4e sou so apduloess wuroa sxe byuasy By. dita 61 avece lovable sue aieve.e 67, 68 
robber, see asilid 
sarcophagid, see flesh flies 
stable, see stable fly 
PAC MIMIC aL HeInd ae pws a Na meen ei eran, WAG) sys aue ad ei wi. 4 sma Pebsgakes sce > puns due 31, 418, 419, 421, 430 
On any ORE SCA BC PF ODIOSIES /1 OVI QCISIS AES IER’. BAL, Hilig as Sb apis does 8 ous @ 6 oe 2» wleranaingsd Bbe bla aus aude « 7 
Flourensia cernua DC. (Asterales: Asteraceae), see "tarbush" 
POMC aE LCMIMGALET AMAL. 1GIICOSONIGGISSIITG Mee MMe a ocr st eo 6 bceoye wcities tvded x aye.» 9» mayo b vleinrand Sunltord 102, 104 
Forficula auricularia Linnaeus (Dermaptera: Forficulidae), see European earwig 
Formica obscuripes Forel (Hymenoptera: Formicdae), see western thatching ant 
Pormiemiaerien mitcid (iymMenoptera), GCC AlSG ANTS: ei fields kxomyses SEM emer a so rriimrcbk ® elayekenentyalana rea 105 
Foulproodeeneral. micludes American and BULOpeam) a... «jer euescoimans <t'eyna cep vlad dn aalsootenelae, cys 34, 298, 329 


American, see American foulbrood 

European, see European foulbrood 
ORES TT NEU POWO de at Nc oe, ee ee 453, 454 
Fraxinus (Scrophulariales: Oleaceae) 

americana L., see white ash 


APA PEC ACyE OUT OCIMMKE TT OCI ONIG SO1ONI tects Ae isty cs ela falda, © wihie: ace, Gal cn ote 9 4 4a.0 2 0s, + SBinwarar ails lem Ds 93 
Fuller rose beetle, Asynonychus godmani, see also citrus, "root weevil complex" ...................05. 68 
fungi/molds ...... 273-275, 286-290, 297, 308-316, 324-331, 396, 398, 402, 405-408, 413, 414, 433, 456-466 
club (Class Basiodiomycetes) 
Pec OsyCOnT Wiz lane ieee fares Sea Ad. Jis S ants Bet ind Male wv emily gmcser aries Ina 414, 459-462 
Cid OmvCOr 7a E MAOCONACEAL) (Ses Mehr rae.) cht tae eas Laek gulls « etaahatghe 46.ce haus 117, 461 
Te aA I Ge aE fee eh PRS sd usb a isie or eh ave, oa vl inde 8.9 oe. jabegiilugdecs. ahs pason vou Ve 274 
Pasaniltiy WilhOlcurysantnemuiny E USQriusn OXVSPOFUIs . aah ant Haeo = 5 ees wed viele a os 2s om npoueie deans sei 94 
Fusarium [Class Hyphomycetes] 
he PAT TEN UE So a cues ihn SUEY Ce SO One REPESAe 89 


oxysporum Schlecthend.:Fr., see Fusarium wilt of chrysanthemum 
solani (Mart.) Sacc. f. sp. phaseoli (Burkholder) Snyder & Hans, see bean root-rot pathogen 


Se EE en eeu ga hr terri eualen ed os er spn erncbuels ols ue sy ade R sya eGeNSiey Bonded» dows 117, 457 

Soe) ea URE ee eI TIVES BESS fae wee Sonrgs Dacganayririnian-Aamigrt poles are agony aw'> orn, AN 102, 107, 413, 456 

cCalsinemamping oftand root rot ofrediand white pines: 2a. i. i. ce ce eee eee es 456 
subglutinans (Wollenweb. & Reinking), see pitch canker 

PreitonmMnliStae OMGTI UME MEN CUUME TSP, JUSISOFING © 0a ao ooo > wetin mieenils aude wy elie mnsuey & wiaiellend @ aye wie neers 104, 456 


G 

Gaeumannomyces graminis (Sacc.) Arx & D. Oliver var. tritici J. Walker ([Class Ascomycetes 
"Pyrenomycetes"] Diaporthales), see take all disease of wheat 

Galerucella (Coleoptera: Chrysomelidae) 
ee Fee ara) ech vom, fa pp Fne, sUa 4%, oe aye ead wile: say pendecngage jaye, Rolls woes 83 
Bee ates Tg 0 re eee 2 a pec icy R mace jn 2 4 se i ae + Seep adiepeetine ni « 83 

Galinsoga parviflora Cav. (Asterales: Asteraceae), see smallflower galinsoga 


605 


Galium (Rubiales: Rubiaceae) 
mollugo L., see smooth bedstraw 
spp., see bedstraws 
Galleria mellonella (Linnaeus) (Lepidoptera: Pyralidae), see greater wax moth 


Gelis'spe (Hymenoptera Ichnetimonidac) i275 faa cs cn rec tote sera etl en ae ee 399 
Geocoris punctipes (Say) (Heteroptera>bygacidae) (7. Soe ae: ie eet es cae 30, 31, 65, 130 
Geometridae’ geomewid(s) "ey eat ee ecco as oe ce tc oct ean 415, 416, 427 
“sipsy moth" (see also gypsy moth) 297 22 asad cds hee ete ale oalaystste ant emetic ra niet eet eg ae ae ee f 
Gilpinia hercyniae (Hartig) (Hymenoptera: Diprionidae), see European spruce sawfly 
"glabrous cabinet beetle,” '7rogoderma glabrimins . Av sin sane ois ane Ne A eae te een eve eee 69, 328 
Glena'bisuica Rindge {Lepidoterar Geometridae)mrey Daca. aac os aes eae ae ie alee tee ae eee 416 
Gliocladium virens J.H. Miller, J.E. Giddens, & A.A. Foster [Class Hyphomycetes] ...... 93, 94, 96, 118, 464 
Glischrochilus vittatus (Say) (ColéopteramNitidulidaé)' se \\2 cal eee nae oie g ete ee eee 535 
Gloeophyllum ({Class Basidiomycetes] Aphyllophorales) 

mexicanum (Monit!) RyWardén's 24s. (.hosga ee ven Cal Seas ae ee ee ene eee 463 

sepiariune(Wulfen:Fr.)'P. Karst) S22 oe ae ele bac oe oe Coe ee 118, 463 

rabewum (Pers Fre) Mutrill 23, cine are ot ea ie oi ee ee 118, 463-465 
Glycine max (L.) Merr. (Fabales: Fabaceae), see soybean 
Glypta fumiferanae (Viereck) (Hymenoptera: Ichneumonidae) .................... 115, 439, 446, 447, 450 
Glyptapanteles (Hymenoptera: Braconidae) 

liparidis (BOUCHE) (28 Fs Ocoee ee Ba PS ARG OTe DUE toa te ee eee 419, 421, 422 

militaris (Walsh) 2442535. Ge Pod VAR Ree Pee Oe RT ee eee ee CH 
Peoat louse," *Bovicola Sp: <<. 20g a Lhe Ab oh end Te eh 6 LN ee epi 
solden-crowned kinglet; Regulus sairapa = ee nt ees ee ee ees oe Caner 447 
Gorse Wl europaeus ee cee ee hy ee Oo eee 21, 36, 37, 78, 79, 466 


Gossyparia spuria (Modeer) (Homoptera: Eriococcidae), see European elm scale 
Gossypium spp. (Malvales: Malvaceae), see cotton 


grain sorghum, Sorg/um bicolor’ 53... 3 oce mule eo es oo ens Ge ee ee Ee eee sae 318 
"sraity weevils,” SiOpHILUS SPD. we-sga/s «0c eres poate eee aa Set ie a Ghee ee rte eee 63 
grand fir, Ablesgrandis* face 00 Oe ot UR EDS: DeLee eee ee ee oe eet ae 452, 454 
granulosis virus (GV) (Baculoviridae) ..................... 70, T1159; 279, 288; 302, 308; 309) 4 5leaae 
of alnrond Moth 2S Aees ese Fe ae he Se Seema ts a ce oe ee ee 219 
of army CutwOrin’ 61) 75 MES ire, cased 6 bk SR ert ee mentee oS ee oe Ok cert ae ey 
of codime mothwst.0...22tt Vere re cee ee eens Cee eC 2 en nee eee ee 320 
Of tall army worm’, Pac, See coe cee ee ene, een eve Te eee eee ere eee ee Ree ner een ate eae 288 
of Helicoverpa armigeras «ii. 254 ine tac e ae Roe SRR Mee Ne Ree te ee ee 288 
of imported 'tabbagewornr ts... cae ee ee ere ene ne Re ee ee 69, 308, 309 
of Indianniéal moth 22h eS 42098 28 Oe Een ee ent es eee 69:70, 277, 279, 280; 292 
of spruce budworm'! 00 Wer 2 be Pee a SE ee Oe ae rere er 451, 452 
of western Spruce budwotm (2346 Sisre «que a ceutiae 2 ee Te ie naira te ems meet ee 452 
grape phylloxera, Dakiudosphaira vitifoliag 2.00 «ten. cakes «Sua de ee ee 6 
grapes ViLiSSpp.” 5 bese Od oe ay Grantee, Saint | Guat ae eek oer) sentir a att Cainer hte cr he tee eee ee 98, 308 


Graphognathus spp. (Coleoptera: Curculionidae), see beetles, whitefringed 

Grapholita molesta (Busck) (Lepidoptera: Tortricidae), see oriental fruit moth 

grass carp, see white amur 

grasshoppers (Acrididae) (see also gregarines, neogregarines, and pox virus) ... 11, 24, 35, 36, 54, 58, 70, 71, 


139, 147, 158, 159, 284, 311-315, 330, 462 
pigmy, see pigmy grasshoppers 


gray Sugarcane’ mealybue, Dysmicoccus boninsist@e 2 eee ae tee ee ee ee ee 8 
"Great Basin tent caterpillar,” Malacosoma fragile incurva qn)... sas 47a ee ee ee 101 
greater wax moth? Galleria me/lonellay oe aoe 32 oe eee 61, 275, 279, 297-299, 411, 445, 452 
green peach’aphigsMyzus Persicae: Sey ele eae ete iter eee 18, 24, 31, 54, 55 
greenbug..Schizaphis sraminuin'.: 1G. ee ee eee Co cee Ce ere eee 10, 24, 54, 59, 129 
gregarine(s) [Phylum Apicomplexa, Class Spozoea, Subclass Gregarinia] ...............0.. 00 eseeeee 317 

It COM FOOTWOIMIS. <5 Oe TAGE Es ow en ee Rome re Bn et les re ne ee 317 


in grasshoppers .%...0 5G 806455 beh Veh Out eee ee eas 
in honey bees 


606 


grubs 
cattle, see "cattle grubs" 
white, see "white grubs" 
Gryllidae (Orthoptera), see crickets 
Gutierrezia (Asterales: Asteraceae) 
dracunculoides (DC.) Blake, see common broomweed 
microcephala (DC.) Gray, see threadleaf snakeweed 
sarothrae (Pursh) Britt. & Rusby, see broom snakeweed 
spp., see snakeweeds 
texana (DC.) Gray, see "Texas broomweed" 
gypsy moth, Lymantria dispar see also multiply-occluded nuclear polyhedrosis virus [MNPV], 
and nuclear polyhedrosis virus [NPV]) ....... eo 1224) 655 le 54-507 56759, 67. 0-72. 101107, 
2052 o-oo. ta loo. 19. LOL, 209) 
301-304, 306, 307, 314, 315, 329, 331, 416-428, 446, 451 


“HVE: s GUEEPON Eg (0 LES AYE T go ccs ly eainte Ue aha ae tea ERROR EOE PRT PO Ca 55, 104, 106, 149 
RITA meV OTT TOD LESCOL nn ene errant In, «wet AER Ose ah ek Rica Giles © ara ETRE Sue's 419 
H 
Habobracon brevicornis (Wesmael) (Hymenoptera: Braconidae) .............. 00.00 cece eee eae 124, 139 
iinorocviusicereaeua (Ashmead) (Hymenoptera: Pteromalidae) ©. ca) cee eo ece et te os tine ce ea 63 
Haematobia irritans (Linnaeus) (Diptera: Muscidae), see horn fly 
PEAT WRNOORIPICC KCI IC OLACSE VELIOSUS Gilets erty cig ey Aiea ey eine he Sok Daa NISRA We Lees 396, 397, 400, 536 
MalemOo mois Oruenr Ol DONC Vi DCES< OCIIUS COUTUICIIS ere woe ae oi oo Gay vs see pa DebSip Apes cor mck ais ois 298 
halogeton, Halogeton glomeratus (M. Bieb.) C. Meyer (Caryophyllales: Chenopodiaceae) ........... 37,18 
Harmonia (Coleoptera: Coccinellidae) 
eG ELLE BEV ESSD,  edy tore guar tlp RRR) SG hag, t- TRAN PO Og.) a 60 
LePage Po aac, phe asedics lst Gus ucit tA iP IPs So ald ne UE a ir Ae Ie eae a a 538, 539 
ARON CCUSEIIICL UCONN SUD mere more er orl N. s a emia Siena? dames sighs uae Gadiialn eat 83 
iteiupoaus venrals tustache (Coleoptera: Curculionidae) 3.0... he be eo de es ee piled wal ew a 82, 86 


Helianthus annuus L. (Asterales: Asteraceae), see sunflower 
Helicoverpa (Lepidoptera Noctuidae) 
armigera (Hiibner) (see also granulosis virus [GV], and multiply-occluded nuclear polyhedrosis 
NILLISH ALN ELY, |) Peers te, fcc Rp Oe Ome Ak ie oa a as ue cas 272, 288, 310 
zea (Boddie), see corn earworm 
Heliothis (Lepidoptera: Noctuidae) (see also singly-embedded nuclear polyhedrosis virus [SNPV]) . 54, 57, 62 
armigera, = Helicoverpa armigera 
/Helicoverpa spp./complex (see also Heliothis (s. /at.), and nuclear polyhedrosis 


Virus: (INE Vera et. oy 35, 54, 62, 63, 71, 158, 159, 279, 280, 282, 288, 308-310, 317-319, 329 
PT AFETIY oo pA gredmeate bs cae Ge ics BE AGG Bem Acer Op nea ORR a eet Aoi ek irae ee 280 

(s. lat.) (see also Heliothis/Helicoverpa spp./complex, and nuclear polyhedrosis 
Vitis RIE!) em eMene ee earn AMEN OLE Neh OR ce Ns. Ok COOP 
SETS T RSE ICN ws ye eile Airs ca eS CEN en CMR RE OrERARS AT SII SCC Pe 310, 311 


virescens (Fabricius), see tobacco budworm 
zea (= Helicoverpa zea), see corn earworm 


iremerobuac ( NCULOPlera merce? ns ieee eee RO tah da heehee eae A als oh Sas Fw 8 gos es 538 
rier ODIus sp meer Optelas LICIMCFODICAC in as asd a ee tle oe ve aicbane Sm cae He a tod A Ed eee vue 8 454, 538 
Hemileuca oliviae Cockerell (Lepidoptera: Saturniidae), see range caterpillar 
BUC RG YSU C ITSO eee ee ee oy 6 oe adit Sa ae Sa ay igs Wb easy fe ALs om 2 scare) sia, we be 428, 438 
western, see western hemlock 
hemlock 
TOA CATIA IRAY ESCEN OT IE JISCEIATIO re iat ince 2 eo hie + oie 8 4 Gea Ha tea wp. Pne pet 101, 116, 438, 445 
Saw COCO I CINES Ue Sena pe ele saat as hoe en hae ce AK Aa ads ayes Salas 438 
hemp 
Dicom aDene (ODOC ne ONO. Mme! Soh re silent? Cole 5. a0 0 towns O88 nba 5 aen ln aes hes 36 
BES AM CSCI ICN GLAM) Bt Aiea fate a egin Sakae Gly pin seer anys wf de Dae so oes aces 77, 82, 89-91 
Pie tatty dV Cri Ol ct CSITUCLOT Wee a tet ee eo ele ew ooh nes Re ey fw nea ine ok nen ae eas ow fete 


Heterarthrus nemoratus (Fallén) (Hymenoptera: Tenthredinidae), see "birch leafmining sawfly" 


607 


Heterodera ([Class Secernentia] Tylenchida: Heteroderidae) 
avenae Woll., see cereal cyst nematode 
glycines Ichinohe 1952, see soybean cyst nematode 
schachtii A. Schmidt 1871, see sugarbeet nematode 
Heterobasidion annosm Fr. Bref. ({class Basidiomycetes: Aphyllophorales), see annosus root rot 


heterorhabditid hematodés, Heterorhiabditidae=.. . +. au. wae ae ee eee 278, 287, 316 
Heterorhabditidae ({[Class Secernentia] Rhabditida), see heterorhabditid nematodes 
Heterorhabditis ((Class Secernentia] Rhabditida: Heterorhabditidaé). -- 2... 70.2. eee ee ee ae oe 68 
heliothidis (Kahn, Brooks; & Hirschmani!976)" 5-3 cue oe ee 316 
Hexamermis ({(Class Adenophorea] Enoplida: Mermithidae) 2) io oc). ctwe act nee ee eee 67 
SDs cpa cane Sh amin, tk as mae cuige cannes Micoe Ate. ohh gOMMENG Tek fica ci et eet ca ae aR eee eae, ae 139 
hickories: Carya Spp.. .. -saussese «sane om aA eeu aaa 6c in ee ee Ot Ree ens 415 
Hieracium spp. (Asterales: Asteraceae), see hawkweeds 
Hippodamia (Coleoptera: Coccinellidae) re sce. os ete o 3) ove cate one aene ooo aces 10 
convergens (Guérin-Méneville), see convergent lady beetle 
ITEAECIMPUNCTAI (SAY) se ois Se i oe i we Oh RR a eo Rance Ss eee a NO 129 Ios 
VOrle gata (GOEZE) "ore = a5 sips eat te rie ie cele tae ee eee eI ee 129137 
Hibiscus'(Malvales: Malvaceae)’ So oe stcck «see oo ae otro © taseaun aaa cee sc ear 62 
Hirsutellathompsonn Fisher ({(Class: Hyphomiycetes| ss oc ca cor ns cae ae ie 287 
Histeridae (Coleoptera)rsee’also beetles, nister a5 a i. hae tee 535 
Homoptera/homopteran oc 0 F<.0 wine warden aug sins 9 8 65 «0 iy ORS Cinna cea ee 159, 453 
honey 


bee, Apis mellifera (see also American foulbrood, chalkbrood, filamentous virus, gregarines, half- 
moon syndrome, honey bee mite, Nosema apis, powdery scale disease, protozoan pathogens, 


purple brood, sacbrood, septicemia and spiroplasmas) .... . 11,19, 34, 69, 71, 72,4571 59e 70: 
273-275, 278, 281, 296-298, 300, 305, 324, 326, 328, 329 
PATTIGANIZOG: rtes ccc ee the ier e es Cee ak Cpe TRRAEENE Sane ORAS Nc Sree ae on ee 297, 324 
bee MILE MACaPAPIS WOOT” viene © cies Aunt We eager oe ce 298 
Mesquite, PPASOPIS STANAUIOSA G Se sysctl oy cere hae, 6 occas eee ee 1], Slee 
Hordeum spp. (Cyperales: Poaceae), see barley 
Dorn Ly? HQC AlODIGATTILANS en cls a he cee ote ae ee ce, ee 25, 35, 54, 64, 321-323 
hornworms, see Manduca spp. 
"Horogenes (Hymenoptera: Ichneumonidac) ©... rss 90. cere Cres ei 440 
house 
cricket, Acheta domesticus (see also rhabdovirus-like particles) ............ 00.0.0 cece cee eeeeaee 300 
Ty, Musca domestica 03 5:2 a.) oe See eee oe eA 10, 64, 321 
human 
genitourinary mycoplasina fi0. 0. acarcs arate Hehe ees ee Ce econ 8 ieee ee 305, 306 
Immunodeficiency virus (HIV) 2) 62 1a ne an Oe se css a cee ee ee 306 
Hydrellia (Diptera: Ephydridae) 
DGICTUNGST BOCK: Soho ae sree ote crete ele atten wha Ree tar a eae 81, 86 


pakistanae Deonier, see "hydrilla leafmining fly" 
hydrilla, Hydrilla verticillata (L. f.) Royle (Hydrocharitales: Hydrocharitaceae) .... 39, 77, 79, 80, 84, 86, 128 
"hydrilla 


leatminingatly,” Hyarellia pakistande wcacta sa. 2.90. Aon wie» spate tee eee ic ee 81 
WEEVIL, BAROUS A/fINIS oe ie dois ye ee ee ee, 80 

Hylemyia seneciella, see "ragwort seed fly" 
Hyles euphorbiae (Linnaeus) (Lepidoptera; Sphingidaé) ... «2 ce ee a ee ee 85, 141 
Hylobius tranversovittatus (Goeze) (Coleoptera: Curculionidae) .7....52.-....40.5..2.000) 0) eee 83 
Hymenoptera/hymenopteran (ants, bees, sawflies, wasps, and allies) .............. 159, 396, 397, 402, 417, 
427, 432, 438, 444 


Hymenoxys (Asterales: Asteraceae) 
odorata DC., see bitter ruabberweed 
spp., see "bitterweeds"” 
Hypera (Coleoptera: Curculionidae) 
brunnipennis (Boheman), see Egyptian alfalfa weevil 
postica (Gyllenhall), see alfalfa weevil 


608 


punctata (Fabricius), see clover leaf weevil 
Hypericum perforatum L. (Theales: Clusiaceae), see common St. Johnswort 
Pa Wistar ec ware OMe eer Ee gore ircne rares gi oy, ANd Beds AVIS 6 Besia & ikea Gen oiatae's a'gap 8 03 oe 8 os 31133) 
Hypoderma spp. (Diptera: Oestridae), see "cattle grubs" 
Hyposoter (Hymenoptera: Ichneumonidae) 


tas eat \TOTCC Re mrmeran r ROR SME eo Fs ese Gh a's, hn) Ss. Sod % Bo doops Hs» enh dus Ae d veep ddiyK's, « 29 
Oy Devas we OCT S ON me Gee ee eae Re Sis raha Gs, e, A aycen >: Kalas, dregs sbPMe sags, a... < quandive sudadec’ 433 
I 
Icerya purchasi Maskell (Homoptera: Margarodidae), see cottony cushion scale 
Ichneumonidae/ichneumonid (Hymenoptera) fog20.. 2... ce ee ee 148, 411, 433, 438, 440, 444-446 
Voninviraanciusa (Hubner) (Lepidoptera WNOLOGONUIGAE) 25. ae vce cyt nee tw ee es cw eee amen ens 415 
imported 
cabbageworm, Pieris rapae (see also granulosis virus [GV]) ....... 3, 6, 24, 31, 32, 55, 69, 302, 308-310 
ivillommleampeeties ( aeroderd Ver siCcQlonamnme its (olin w AGG. cst, ho Slow FAR ad etls x,3 sma vo0,2,003 415 
BaITIOLe CetieCIAIN ata OO (EOUSISISDO Mara. eet ia Wes fi vgdia edie § Gd cs w Sas ale de sug teers Bas Youn 125, 285, 286 
"Indian gypsy moth," see gypsy moth, "Indian" 
Indianmeal moth, Plodia interpunctella (see also granulosis virus [GV]) ............. O91 k 210; Lig. 21, 
BET Nee e eeO CG ee ar ILS meme nem mre er a ee ch eh Si ay Sls ie ee aus duns) Seopa oll aponeoidisse | 317 
TPE CAC OGED NIE 6A WL Vee LD EDLOTe STITILES © Riel egos dojc sagt: feck) 5,30 Siok PREM ove. «5c, agers. 4m wtacs 114, 438, 439 


Ipomoea batatas (L.) Lam. (Solanales: Convolvulaceae), see sweet potato 
Iponemus, = Tarsonemoides 
Ips (Coleoptera: Scolytidae) 

confusus (LeConte) 

oregonis (Eichhoff), = 1. pini 

pini (Say), see pine engraver 


SBR maRbersISCDOCt OS MECN OLA VOL sc arrays) ill < scan eimun Ax Sie eee soshe rn exewiers Bimumc nid’ s 399, 402, 403, 405, 409 
MiGeseen eeriis( es) ( clo viricac) newer n Oy ni aenaes eae | eateries EM Wier cya ie cn 6 ks oie 2 Saco a 294, 300, 414 
PEECSS C11 LLCO ramen a Per cot) eeu ASUS) Sie Gh, che cUGME COLA opm pe 6 hos lo west av 5AR mye 294 
Bol orn CO Gal wt OF) Meme a Grey reg. ice», oft, tCake te eas, CaM nn eon a pce wan thos! wi udhpiiens noenie« 300 
Irpex lacteus (Fr:Fr) Fr ({Class Basidiomycetes], Aphyllophorales), see white rot of wood 
PUG At Class El PO OMVCCLES)| )mmeta sere ce yec oe alekess woe a, olaiei sais 2 FAs he tik 9 nae «aya npn beta aia oid A tur 316 
SOLO MILES UIITEHS CO ASey yl © OLGOPteTasFUIS(CTIGAC) lnm © 6,2 <0 «vile toys Grail tenure. vias, 4, Kins vie % sadhana seal o ars 535 
Isoptera, see termites 
PUA ATINETISEIC MCE ON CG HIES DY CROCCUIALUSMMN EE, «vic a cetcis 1s. 6 dosnus agent nyse os 6%, wie fe nite) 9.08, So lagi MEd 36-38, 76, 78 
Itoplectis (Hymenoptera: Ichneumonidae) 
SPICE CLOT SUSAN) EMMA, ole) efyp eens Voile 27342 ax sein et dn Saeed anutasa dary opiate he W'Bs.ske oldopiS. pee Oy Ad cae dent 439 
AGGIE (ETONSUCICE) ia « Belli ale Meee ye oid casas elt ed epean ll arti dinuedaiad > temps 110, 410, 445 
J 
Sa CMNSIDE MA AIIEIS AIEISE AI) CLs occ ee cece see ne ae SOPs nese EA Can (ote ace SE bees nee sts act 411, 439 
ReaC Haine uC Ofilia OOLISTONCHIG PUES eae ari Feels nin Qe Sok Sale oe) os tuna ska Shr Sot none dine 115, 439 
DANY ares US ody CELeLCLOPICT a; BCTYUGRE) if. casa neg iran «Busi Aye on Fins 5 saute eat sony? + laine wsogoge 3.2 


Japanese beetle, Popillia japonica (see also milky spore disease of Japanese beetle) ... 8,9, 11, 12, 16, 19, 20, 
34, 55, 68, 73, 157, 158, 270, 289, 290, 296, 298, 299, 315, 316, 331 

TsO Weed nL tem AS QNTA ILI aaMiarete cite MOREA Y Fae COM LAND NS + riage shale Bias tie voRaiapaie’ A eisiase mcs ais 89 
Meme COAt CIA eMe tCOODSICVINGIICH EA tan, oocyte ten cit its ete be ete t eee eee snte rene se 90, 91 
jointvetch, northern, see northern jointvetch 
Juglans (Juglandales: Juglandaceae) 

nigra L., see black walnut 

spp., see walnut 


FOI pine spiders poallicidaema ie mii-\eamie ital hl AGIAEh aac se hee nee wee tiie eee nee cow tig omnes 448 
Junco hyemalis (L.) ({Class Aves] Passeriormes: Fringillidae), see dark-eyed junco 

“Tpit kote ae TEV IE TaN ai Sige) af fs Res ee Reo a ei eePaP ve = ere 413 
BUT PEL (Ste UI EEU SDD Arey tee sas ofa See) S ole m1, er he ns morse naennthok en eH ang en 412, 455 


Juniperus spp. (Pinales: Cupressaceae), see juniper(s) 


609 


K 


Karpinskiella paratomicobia Hagen & Caltagirone (Hymenoptera: Pteromalidae)....................- 398 
khapra beetle, Trogodéritia Qranariurn |. sven taper a nls yo sans 0 apn 5 eee oes oe aie eis oe 158 
Klamath weed, see common St. Johnswort 

knapweed, 


diffuse, see diffuse knapweed 
spotted, see spotted knapweed 
Russian, see Russian knapweed 
squarrose, see squarrose knapweed 


knapweeds,, (see: also.Ceniauréa. SDP. )\er ann eeu gait se a ane ey i 76, 78, 79, 83-85, 90 
"Koster's curse,” Clidemia Wirtd ahs .cs% sth ee eb ODay tate ie ee ee ee 466 
L 
Laccaria ({Class Basidiomycetes] Agaricales: Tricholomataceae) 
lageaia (Scop, ex. Fr: );Berks: &. BY, sceasc aim iyo RiuMiangs cua 116 «5 © ol Caio an 461 
bicolor. (Maire) Orton, 2s 3 2 ie ak eee oi ey eieren cans 2 vaya got edo eure ao alee a) 414 


Lacinipolia renigera (Stephens) (Lepidoptera: Noctuidae), see bristly cutworm 
Lactuca spp. (Asterales: Asteraceae), see lettuce 
Laetisaria (\Class Basidiomycetes |. Aphysiophorales) . 25.) ¢.+<. sale eae yee se oe 94 
Lambdina (Lepidoptera: Geometridae) 
fiscellaria fiscellaria (Guenée), see hemlock looper 
fiscellaria lugubrosa (Hulst), see western hemlock looper 


lantana, Lantanaeamara Lo(Lamialés: Verbenaceae) <5 ae 2: ara oes serene ea crete ee rz 
Laphria gilva (1...) (DipteraxAsiidae ie dae. terre ern ea ee i eee ee ee 400, 535 
larch, Larix'spp..(Pimaless Pinaceae i career sie are sie tee eee ae 117, 421, 441-443, 462 
western, see western larch 
larch 
caséoealer, Colcopnorajaricella®. 947.1: ae eee 8, 15, 18, 55, 56, 101, 104, 107, 114, 161, 439-444 
SdWilys.PristiphOrd CriChSOnlg mol ake ck @ cence CEO Oe Cea eo ee 102, 114, 444 
large aspen tortrix;,Choristoneurd.caryliciqnd’. 2. . 25 eich weie ae: ks a cia ee 112, 428 
Laricobius erichsonii Rosenhauer (Coleoptera: Derodontidae) ..................00005- 453, 454, 537-539 
Larinus (Coleoptera: Curculionidae) 
curtus HOcnhnut. hese Demeqscem gine gehts op ste 5 oy abe aia leunniite ar tetas rah UCotere Went Siar et nen 84 
mninutus Gyllenhal «ce oak Donte oe tee erates eee ever lela a cae ene enc eee 86, 140 
obtusus’Gyllenhal | o ics5% fagucttig plone ate soca Sie elves faces Sagan 86 


Larix (Pinales: Pinaceae) 
laricina (Du Roi) K. Koch, see tamarack 
occidentalis Nutt., see western larch 
spp., see larch 
Larrea tridentata (Sesse & Moc. ex DC.) Coville (Sapindales: Zygophyllaceae), see creosotebush 
Lasconotus complex LeConte (Coleoptera: Colydidae) 3-5) ot ne es ee 535 
Lasioderma serricorne (Fabricius) (Coleoptera: Anobiidae), see cigarette beetle 
Laspeyresia spp., see Cydia spp. 
leaf 
blotch, see Septoria leaf blotch 
rust, see Eurasian poplar leaf rust 
spot, 
alfalfa, see alfalfa leaf spot 
poplar, see poplar leaf spot 
tobacco, see tobacco leaf spot 


leafhoppers (Cicadellidae) so aL raters: syne aim ese ce cet ee 54, 62 

EMPOASCO? udu ih Saalintsby a so oa ged nt Ga gece aks a oe ore ee ee 54 
leafy spurge skuphorbigesulomers ee. ee ee 76-79, 84, 85, 88-90, 124, 141, 150, 162 
legume/leguminous.crops,(Fabaceaejz ch 2 nie ernie ee ae ee 28, 98, 308 
Leiophron uniformis (Gahan) (Hymenoptera: Braconidae) ............-.-..ecrcseccccetcvsseerst ly 63 
Leis. dimidiata (F.) (Coleoptera; Coccinellidae) giry.aaame ive ok te eee ee 539 


lemon, see rough lemon 


610 


Pemopiacus curiuss ownes (Livimenoptera: IChNeUMOMIdAe) os dpc s cee cas eee ee a awe de owlk ele eens 140 
Lenzites sepiaria, = Gloeophyllum sepiarium 
Lepidoptera (butterflies, moths, & skippers)/lepidopteran/lepidopterous (see also protozoan 
pathogens) ....... eee O2, O9f 11 2109) 270,212; 210,282,293,.300) 308, 315,317, 320, 321, 
409, 415, 416, 427, 428, 430, 431, 433, 439, 444, 448, 451 
FIG area eta ee eee ae dM WON SANTOR AA AEH co) ain eu is sre. oe ga bin Ha Ais a inopagerp aye'm siete > 409 
PUT ec RT MN Se Eh 0 oy Uas dna. given. & Wa 40 a alk oro pw dindleLeee ln 409, 410 
Lepidosaphes conchiformis (Gmelin) (Homoptera: Diaspididae), see fig scale 
Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae), see Colorado potato beetle 
ese Me HOU MOIOdUSIC (OCW) UIDLCL om ACOUMICAG NG cca oe ph kx a 6 xk Coles «ORS Mw 4 ow GRAS ee endo 3] 
espesrarcruinvord (REY) Mp LCKa Mm NACIINIOAS | ears Ate eg mila ove G asus aa oie e c's «ed es dk mabe we 30 
le sere e alte BiCartti itt] tinfoil meen ne SE Se fe eg ace ii ake ia Malka due. 4 ved.0i0.9) Hye Gay, 4 Gwiseeeue aod ae ac 88 
ROLHICE MIICLICIS DL) ane Cereal UA Tan x dil apg eS <n eA 4) e Brdswgs Gs onece a ue 10,271, 299 
Leucoma salicis (Linnaeus) (Lepidoptera: Lymantriidae), see satin moth 
Leucopaxillus cerealis (Lasch.) Sing. ({Class Basidiomycetes] Agaricales: Tricholomataceae) .......... 459 
Leucopis (Diptera: Chamaemyiidae) 
eC (PALIN) ete te eee Me Wee er cc VATS ee eae orks oud aia on SI w dee Spe aie Bin Daksa He 538 
ROY ATS OTOL SI 5 al Ss a Gal er ar tn rea Oat tO vn a ee aera ee 129, 138 
VIET Mg EU Ere oR able SI gee ecient Reape) Seater mene tree aa 453, 454, 537-539 
SPO eS ade hs PO OE, RE Ae Bae Ce Sr 539 
5S Emre I Mee Sete ese cay gl ae (eo CSIs etch ae Senile ee mds Bunua so) auch Gasuetie ® Sond mid 538 
lice, see "biting lice" 
Ning porets aWAaSHDOTCOIE OOOSESIC SUTINGOE Melee Agave Konus GG ds sk UF ta: mn, ook Guage oP ww ities 413 
Bie AEN OGL CE mE TIC) (cu CR CME! Ck rene Me Rene \aintss| Sey oaF ahaa oe ena W plas alavstinige’ taua Alsi a, Side» & 16, 25 


Limonius californicus (Mannerheim) (Coleoptera: Elateridae), see sugarbeet wireworm 

Linaria dalmatica (L.) Mill. (Scrophulariales: Scrophulariaceae), see Dalmatian toadflax 

rec tecme RING GeM TECOLIIELCT US ULC Men anaes aie tne Nel ay ee E aud aco “ally le yn 5 wus ee Mh HG, Hed eA kes 24 
Lipaphis erysimi (Kaltenbach) (Homoptera: Aphididae), see turnip aphid 

Liquidambar styraciflua L. (Hamamelidales: Hamamelidaceae), see sweetgum 

Listroderes difficilis Germar (Coleoptera: Curculionidae), see vegetable weevil 

"little leaf notcher," Artipus floridanus, see citrus "root weevil complex" 


RTICIeANICISC SOR MV LODIMNMOlO CINMONIOM | were echt cd Sass 4.» a 2is aim > Gis ond ce « sy Ae Rieatalend un yard 104 
mopnara cla cae(.Ownsend).« DiIptetan LACNIae) x cts gw yseusie vee yr wn oe ati wwe wrens le, dice alle = 2 Re 61 
POD al Vapi ect QCA a net oe ree cde eee asec so elon eRe eo iR aw ss hy, we wipe mynd nod 405, 407, 455 
bes FOIE ITE MING AL VIDOR MICE! CUI By ate tsa asic ia gel nd Sa tease sas hha Se as cis Sou se eae « 116, 455 
Cris tomes COC ULAG Ame Mier Soma NE Ss Gee oN Gi aon! $75 Wins Gudea Ye ew «> Wia\eMee ayn ite > Wim huece aicidt events 312.314 
LOIDeNO lee MINUS COMMOLIG etic calc vii mals ws ee Aes Deel oer eye oN aiap)''e len MA 397, 399-401, 535, 536 
onc HaCd JIrIOGna WieiSen KDIptera LONCHACIOAG) ths whe Md: warts apals Pele tis ys Hote ots wie ole Bi aid dys, gevese avatar 535 
Perri raeiiiae | LIIDteT a ) eee Mareen s Meroe Ve Nr IAN. 2 ete RN GD Ara i A US Ay heed aca dee oe 535 
Longitarsus jacobaeae Waterhouse (Coleoptera: Chrysomelidae), see "ragwort flea beetle" 

MMYG CALC yelcl 70s ee LSLT IS, 5 eke seats leks! a oNeas airpeN chests) atte iar 2 eas anson nai ishey aya (0h pit 0, oe, 8, he's 9 wi Bee 395 
Lophyroplectus oblongopunctatus (Hartig) (Hymenoptera: Ichneumonidae) ....................0005. 438 
POU ADIITAC CHG AS Alitalia es Mee eee aris ees ie orl ie Vliccruget utah gush ew poll did SAK (eh ctndicm 9 smn oh 465 


lowland white fir, see grand fir 

Ludwigia spp. (Myrtales: Onagraceae), see waterprimroses 
Lycopersicon esculentum Mill. (Solanales: Solanaceae), see tomato 
Lycosidae/lycosid (Araneae), see wolf spiders 


vaca thompson Hering (Diptera, Tachinidae) «4a... my o miwiale 847) 2 dmineisidinnn'e «/oe snc 18, 124, 139, 291 
BO Uise US 1S SDD rer ee eet rah ET arc aah eho fois al are pracy ad 24,25, 29-31, 54, 56, 57, 59, 63 
Lygus (Heteroptera: Miridae) 

es erie. ell Olt meme et ae ee tear fide Minha a Beli os Ghai ag ia tiaras wa iningals Ss 9 das, bo 31 

lineolaris (Palisot de Beauvois), see tarnished plant bug 

spp., see lygus bugs 


Lymantria (Lepidoptera: Lymantriidae) 
dispar (Linnaeus), see gypsy moth & "Asian gypsy moth" 
obfuscata (Walker), see "Indian gypsy moth" 
feveniamtriaase IyManiriid(s) (LEMIAOPteIa)i sos... wwe ns er ee dee se me Pe 2a te ne eens Sele Hele 416, 433 


611 


lynx Spiders, Oxyopidae |. .ai 2 i .iccucn + Selene cutie 2 Ge ee ioe Fn een Semen Ones cee 412 
Lythrum salicaria L. (Myrtales: Lythraceae), see purple loosestrife 


M 
Macrocentrus (Hymenoptera: Braconidae) 
aneylivorus ROHWEP MO aot ce cao sca 8 oem sue neh wa orig] ge a ote ae 10, 19 
grandii Goidanichy? ape ok eae hha tao ees ae ee ee S12), [soe 
linearis. (Nees) Se Sens ac cite hit age pride e ece wclyl oie om wi ake alee ee Ler eae er 139 
Macrocheles boudreauxi Krantz ({[Subclass Acari] Parasitiformes: Macrochelidae).................-4. 406 
maggots anthomylid 024 20iRS Sid). wine sana ne ieee eaig go ye cee oe ne 54 
maize, see corn 
Malachius ulkei Horm (Coleoptera: Melyridae) 1. 2 sic ee cate oe = eee ae ie en 1125-427 


Malacosoma (Lepidoptera: Lasiocampidae) 

disstria Hiibner, see forest tent caterpillar 

fragile incurva (Stretch), see "Great Basin tent caterpillar" 
Maladera castanea (Arrow) (Coleoptera: Scarabaeidae), see Asiatic garden beetle 
Malameba locustae, see Melamoeba locustae 


malariay Plasmodium gallina@eumys, : Dae phew: sates ca ces 4 ae lg oregon ghd sn ae eee 284, 294 
Mallophaga, see "biting lice" ; 
Malpighamoeba mellificae (Prell) (Amoebida: Endamoebidae) .............. 2.000 e ee eeaee 72, 324, 328 


Malus spp. (Rosales: Rosaceae), see apple 
Mamestra configurata Walker (Lepidoptera: Noctuidae), see bertha armyworm 
mammals (Glass: Mammalia law... oe ees aa oes ee eae ee 436, 439, 444, 446, 462, 463, 466 
Manduca (Lepidoptera: Sphingidae) 

quinquemaculata (Haworth), see tomato hornworm 

sexta (Linnaeus), see tobacco hornworm 

0) 0 lee ea eee Se een re Are Cea Nem gr re me RS Aa RA ee phe 
maplés;‘Acerspp. 21 ene. SPER oe 65 obama 'e 9 ahecein usecase a7 on ra ee te ee 118 
Matsucoccus resinosae Bean & Godwin (Hompoptera: Diaspididae), see red pine scale 
Mattesia ([Phylum Apicomplexa, Class Sporozoea, Subclass Gregarinia] Neogregarinida: Ophryocystidae) 


geminata Jouvenaz & Anthony noel nak Ao ws e ARE IC Ge a hiak Gn <n oe tus aa ee 286 
irogodermae Canning nei ne sis sx teak ou elas heii Shean tal | claude weg ea ee ee 327, 328 
Mayetiola destructor (Say) (Diptera: Cecidomyiidae), see Hessian fly 
mealybues (Pseudocdccidae).3 Vai y Sa: cone a ek oe obeep ce © Br cee nea ae tee 10, 62 


Medetera aldrichii Wheeler (Diptera: Dolichopodidae) 
"medfly," see Mediterranean fruit fly 
Medicago sativa (Fabales: Fabaceae), see alfalfa 


ie Geo S 8S ORME S Soe Ree Ree = 3914399 Soe 


Mediterranean 
iriit, fiy(medtly™), Cergilis can inilain ee. ae otal ak fe es 16, 63, 68, 267, 278 
sage) Salvia aethiopis Wa. See caw ncit ire ae amt GR PARR eC Oe ea eee a 36, 37,78 
Megachile rotundata (Fabricius) (Hymenoptera: Megachilidae), see alfalfa leafcutting bee 
meélaleucaMelaleucaquinquencrvia see: 2 ode hice ee eee et ee ee 711,49, 80, 147,458 
Melaleuca quinquenervia (Cav.) Blake (Myrtales: Myrtaceae), see melaleuca 
Melamoeba locustae, (King & Taylor) ([Class Rhizopodea] Amoebida: Endamoebidae)................ She 


Melampsora laricinipopulina Kleb. ([class Basidiomycetes] Uridinales), see Eurasian poplar leaf rust 
Melanchra picta (Harris) (Lepidoptera: Noctuidae), see zebra caterpillar 
Melanocallis caryaefoliae (Davis) (Homoptera: Aphididae), black pecan aphid, see aphids, pecan 
Melanoplus (Orthoptera: Acrididae) 
bivittatus (Say), see twostriped grasshopper 
differentialis (Thomas), see differential grasshopper 
sanguinipes (Fabricius), see migratory grasshopper 
Melissococcus pluton (White) Bailey & Collins 1982 ([Class Bacteria] unplaced genus), see European 
foulbrood 
Melittiphis alvearius (Berlese) ({Subclass Acari] Parasitiformes: Laelapidae) 
Meloidogyne ([Class Secernentia] Tylenchida: Heteroderidae) 
arenaria (Neal 1889) Chitwood 1949, see peanut root-knot nematode 
spp., see root-knot nematodes 


612 


Sree ME SRI CIROCEECHCHCIIMEILAG mnt tert s 1 Noh 8, cs eins Miele wih aa Vd alee Ria bey oR Ae ES be 16, 63, 68, 278 
"melon fruit fly," see melon fly 

Melyridae (Coleoptera), see beetles, melyrid 

Mermithidae, see mermithid nematodes 


mermithid nematodes ({[Class Adenophorea] Enoplida: Mermithidae) ......... 33, 66, 67, 286, 287, 294, 316 
WMesoleius tenthredinis Morley (Hymenoptera; Ichneumonidae), «2 ..05, 02-5 dee. ee ccc ce cee 444 
Ie SOIC ET ONODES LL OF len ce pee eee wie RT EA hes ofae Abe Aetna es oles Sain we os oh 1M 
honey, see honey mesquite 
Pisetal Mantel MOCUIGMMOUIs Wet ICTOINCC hs sau issn ss Seed wks Ws eue ss ced ae 110; 412413 
Merapniaipnus aeneolus Curtis (Ataneae, Salticidac) fy. ce ss. s cesses bbe tee heen esr ccees 435 
Metarhizium anisopliae (Metschnik.) Sorokin ([Class Hyphomycetes]) .................... 316, 331, 414 
MerER Oasis) sUL eras Ss yIpMIGGO) weet te Gory ne ke hase ee eee ste pS cea dee bed a Chee 538 
Metopolophium dirhodum Walker (Homoptera: Aphididae) ........... 0.0.0 ce cece cee eee 59.161 
Mrecizneria paucipunciela Zeller (Lepidoptera: Gelechiidac) 24.2... 0 00s Pb ee ec ees 85, 140 
Mexican 
bean beetle, Epilachna varivestis (see also virus-like particles) ......... S, 10172.) 1 50,158, 60) 61; 
121, 122, 127, 138, 146, 299-301 
VCAY MAMASIV CD NUUCHS mints en ye he ok ee ee Pa te ta seth oa ns es 128-130 
RIC CIOOL EIB OF Cll Cll Of Li) te I EI SR yy aS dnc oe ME oS oe a ea Petes Dba ss 128 
Microctonus (Hymenoptera: Braconidae) 
Ce MOP OIC SE LANaI) meme aa eet eetome TOURS aia 6 isa vies) Goh ols a a ee ae eS a ede see ae CLP ORa Bre) 
COCR ICE MT er te ee ON NE ea cals cs Meas ee Pek ech ae eee bak 6 Ste 12201358 
CHUA BUG GENIC 3 Ege RT, MO (ite olin a das a a ae a a ee a 138 
Pere GO DetadLepiGOplctd Miu n ane Skt wie oate a pe ekle San eee ha ate ety ates 4 ele at 101, 116 
Microplitis croceipes (Cresson) (Hymenoptera: Braconidae) ...................... 30, 31, 62, 65, 66, 289 
Microsporida/microsporidan ({[Phylum Microspora] Microsporida)...... 35, 71, 277, 283-286, 288, 291, 294, 
295, 312, 313, 408, 415, 452 
DOW OLD iceeiiny Wate a Perera Veta Pel Sie) fd acnels ipteetsaiate alibi aie ec ely aiec wwis ane woke sche v4 285 
Micnoerysiavus (Moward) (Hymenoptera, ENCyitidae) uciiwaies sc Hatisunesivis oh bes et eee ce en es 32 
Mn GratcrueetassGOD Pere fel anoplus SANCUINIDES pa wkn. a> Pe) ae ees Oe CA ak Bes pees bbe 0 312 
Mikoletzkya pinicola (Thorne) Baker ({Class Secernentia] Rhabditida: Diplogasteridae) ........... 398, 536 
RUMNMELE SICILY OLA ICT IOTIII Pett ee EN ee ss oe the eine ne eae aes Wcle eh 8 6 otis bate S123 60) 8. o2 
milky spore disease/milky disease of Japanese beetle, Bacillus popilliae........... 12520, 34; 157, 289, 296, 


299,315,516 
Miridae (Heteroptera), see plant bugs 


Mstie 0es (Olan acede my IsCaCcac) ma pireta ey than ee. ose eae he hohe SG alee he es 465, 466 
dwarf, see dwarf mistletoes 

mites [Class Arachnida, Subclass Acari] ......... 45, 53, 56, 62, 69, 73, 83, 84, 102, 108, 109, 277, 282, 297, 

298, 328, 329, 350, 395, 398, 403-409, 446, 448, 449 

Bryuntaciu.( ParasitiiOLmesvEtyUIraclae) Gamers ibe eeu na ech ee os ses eee thee Rb sae Hee 449 

miesostiomatid (Parasitiformes: Suborder Mesostigmata) 22.2. eet ce ee ee ee eau eye. 408 

PycmOrcCA GamiOlinies; PYCMOlGAC) Werte aa Nt hee oe hea ace Hetkn Neko s ee eet oi ees ee ts 408 

Poi era Mc anivOests Lean CHIUAC) Gm meneer a ete Mis fo fhe tie). re Mt tl a Pe ae he Nace et see bs os 56 

Far OUeNGM Ac AtmtOrmneSs al AISONCMUGAC) 2 te. owe tas. c devs e seme Sat vu yas oma ene e ates. 408 

TERNS CRLE os Gerd eee who Sle o oi erating ange col ge nY rom MON RE ep PSE REAR NLR 0 a ean aC 297 

WEITERE ESC) oo Sk gl oro ype ee ae EN i SP See areas eg re a nr) 305, 306 


Monellia caryella (Fitch) (Homoptera: Aphididae), blackmargined aphid, see aphids, pecan 

Monelliopsis pecanis Bissell (Homoptera: Aphididae), yellow pecan aphid, see aphids, pecan 

Monilinia fructicola (G. Wint.) Honey ([Class Ascomycetes "Discomycetes"] Heliotiales), see brown 
rot of peaches 


Monodontomerus dentipes (Dalman) (Hymenoptera: Torymidae) ............ 0.00. c eee eee eee 114, 439 

ArasastC HUST IIOEY Pal) WLONOMCIIGAG) decisis, sae Sakis oe yue Ung oon mw hasan Abana cosie ais 4a ngniae hos 13 
Morator aetatulus Holmes (Picornaviridae), see sacbrood of honey bees 

PASEO RIG Cet Wari IES 817071 CR rt ok lh cS eae got eons pai niogsviliy hs) Mis) ont ayn Gp] 4 pot RBHoy dle As 3.13 

mosquitoes (Culicidae) (see also iridescent virus) ............ 33, 35, 64, 66, 67, 70, 71, 158, 159, 276, 281, 

283-285, 293-296, 305, 310, 321, 322 

anopheline (subfamily Anophelinac) ............ 0. 6s cence ee ee eee eee e eee n eens 70, 158, 284, 294 


613 


container-inhabiting osic5.<e5.03 6 oS etiel so sl soon cutie early SE ue aie) Pile re ae ae 284, 285 


TlOOd Water ce. Sc Su Bu hike puck cc oecee so hedel yh doce Gee eee SALA pore, Oot ec 294, 295 
ricé field... 0... ccs bse eeu es oy ne 4 oe We ilaiein Gite Cia a 5 Gps ae nen cohen ata caer ae a 225 
saltmarsh << cs. vise a sleie asm. seine es Sb RUS whe ds ee aya Sh ale a/c eae Als le een 295 
mountain 
chickadee, Parus gamibell o. o.. s+ «6/5 <)n aPcuap 2) soeneibesispladls oye la ennai rasa ae ee 434, 536 
pine beetle, Dendroctonus ponderosae....... 102, 104, 105, 108, 109, 397-401, 404, 405, 409, 535, 536 
Mucor piriformis E. Fisch. ([Class Zygomycetes] Mucorales), see Mucor rots of apple and pear 
Mucor:rots of apple and pear, Mucor piriforimis) oo. ec sss + a Milas lea ike een ee 98 
multicapsid/multiply-occluded nuclear polyhedrosis virus MNPV) ..............055 35, 300, 302, 308, 311 
of alfalfa looper, Autographa californica MNPV, or ACMNPV . 70, 270, 271, 279, 280, 282, 299, 302, 308 
of cabbage looper, Trichoplusia ni MNPY, or TOMNPV 2.3 10. ata ee ee 300, 302 
of celery looper, Anagrapha falcifera MNPV, or. AFMNPYV sce ais an ots 6 oes esl Seen 308, 311 
of Doug!las=fir tussock moth, OPMNEPV “2.8. aay eit ent oy-s eee dye hs eg 437 
of fall armyworm, Spodoptera frugiperda MNPV, or SEMNPV ........ 00006 cece cece een ee aee 300 
of gypsy moth, Lymantria dispar MNPV, or LAMNPV ........... 00 c cece cease 302-304, 426, 427 
Of HeliCoverDa GFMIGera i. 5 ccm tees sees oes © 4 eis waa hy ve eis Hale a+ SNe in ae pene eee er 288 
of yellowstriped armyworm, Spodoptera ornithogalli 0.055 3.1. ws os eect 308 


Musca (Diptera: Muscidae) 
autumnalis De Geer, see face fly 
domestica Linnaeus, see house fly 
Muscicapidae ([Class.Aves], Passeriformes) 2c. 0) 023. siels spas eeeacieiie os aie ae 536 
Muscidifurax zaraptor Kogan é& Legner (Hymenoptera: Pteromalidae) ~. 22.02: yam. a eee 64 
Muscoidea (Diptera), see flies, muscoid 
musk thistle’, 
Carduus NULGNS:SUDSps [eIOPR VIS ees scare ue pee 37, 38,.76, 77, 82, 83, 89,90, 161 
Carduus nutans subsp. macrocephalus 
Carduus nutans subsp. nutans 
Myiopharus (Diptera: Tachinidae) 


doryphorae (RUCY) sive occ stacks reels ach soleus akeaeica ds, kateb iets catcor Grist ode one 139 
SPs 5 ns sig a ie.0 doe 9 onagetion agua cae Afi aN Es gid cuelta oa age altar ee Hee aR RM tcc Geri dil, fg tea ie Oa ae 139 

Mycoplasma mycoides ([Class Mollicutes] Mycoplasmatales: Mycoplasmataceae), see bovine contagious 
pleuropneumonia 

mycoplasma(s) ([Class Mollicutes] Mycoplasmatales) jem cr. eer oe ne ye ee 305, 306 
human genitourinary, see human genitourinary mycoplasma 

mycoplasma-like organisms (MLOs) ([Class Mollicutes] (proposed genus Phytoplasma) ........... 306, 458 

Mycosphaerella populorum G.E. Thompson ([Loculoascomycetes] Dothideales), see poplar leaf spot 

Mydaestes townsendi Audubon ([Class Aves] Passeriformes: Muscicapidae).....................000- 536 


Myrica faya (Ait.) (Myricales: Myricaceae), see "firetree" 

Myriophyllum spicatum L. (Haloragales: Haloragaceae), see Eurasian watermilfoil 
Myrmecomyces annellisaes Jouvenaz & Kimbrough [Class Hyphomycetes) 
Myrothecium verrucaria (Albertini & Schwein) Ditmar:Fr. [Class Hyphomycetes] 
Myzus persicae (Sulzer) (Homoptera: Aphididae), see green peach aphid 


N 

Nantucket pine Up. moth, Aiyacionia frusiandon das ne ie ee oy erent an ee 8, 110, 410-412 
Nashville: warbler, Vermivora ruficapillay 2 tac dicucteun de socks) 9 cekte tie cae pode eke ee 434 
navel orangeworm, Amyelois transitella (see also picornavirus, protozoan pathogens, Rickettsiella, 


anid RNA, VituSes ) sca sa st ce eS eae ise cat cee oe a 18, 36, 68, 70, 71, 276-278 


* The correct taxonomic name to be used for the majority of musk thistle populations in North America, 
according to the rules of botanical nomenclature (J. H. Wiersema, ARS Systematic Botany and Nematology 
Laboratory), is C. nutans L. subsp. /eiophyllus (Petrovic) Stoj. & Stef. (= C. thoermeri Weinm. sensu Kazmi 
[1964] or McCarty [1978]). See also Moore and Frankton (1974) and Desrochers et al. (1988). Some releases 
against musk thistle in Montana and Texas, and some collections from musk thistle in Italy refer to C. nutans L. 
subsp. macrocephalus (Desf.) Nyman. 


614 


Necremnus (Hymenoptera: Eulophidae) 


ee Ol NCOs) Peer men ea ce ga he so as fn ie Bias aolat MA ee ts oes le ea 138 
EU AIR Ol en en ee eine eS ite ie lc ee coe viacete te eae ns tate bc his bebe bs 442, 443 
Mierimeiimiers aU CCeraIsGinneaUnmINeTs) Ge vers a ag ctr ah ts Pies Paice ate os whe elds 110, 440 
nematode(s)/Nematoda [Phylum] ............... LOFT 27 1921335. 39,00, 79.91, 101,102, 108-1105 116, 


164, 165, 277-279, 286-288, 294, 307, 312, 315-317, 327, 331, 
395, 396, 398, 401, 404-409, 412, 413, 452, 453, 456, 458, 462 
heterorhabditid, see heterorhabditid nematodes 
mermithid, see mermithid nematodes 
rhabditid, see rhabditid nematodes 
root-knot, see root-knot nematodes 
root-lesion, see root-lesion nematodes 
steinernematid, see steinernematid nematodes 
Neoaplectana ({Class Secernentia] Rhabditida: Steinernematidae) 
carpocapsae Weiser 1955, = Steinernema carpocapsae 
glaseri (Steiner, 1929), see Steinernema glaseri 
Neodiprion (Hymenoptera: Diprionidae) 
excitans Rohwer, see blackheaded pine sawfly 
lecontei (Fitch), see redheaded pine sawfly 
pratti pratti (Dyar), see Virginia pine sawfly 
sertifer (Geoffroy), see European pine sawfly 


swainei Middleton, see Swaine jack pine sawfly 
tsugae Middleton, see hemlock sawfly 


Neodusmetia sangwani (Subba Rao) (Hymenoptera: Encyrtidae) ........... 2... ..0 0c cece eee 27 
MOnOTGr ante NCODTCEALIINGA oh ut aa. oe oes Lehi 6 ok SET Bae Rete Se ee ces 286,3127327 
SOT ASSOUDCLS Mrmr ee ee ee eee ee SSE tie iso tts aE to SRS Abt Pete ee a he das 312 
Neolentinus lepideus (Fr.:Fr.) Redhead & Ginns ([Class Basidiomycetes] Agaricales), see brown rot 
Neoparasitylenchus scrutillus (Massey) Nickle ([Class Secernentia] Tylenchida: 
PEM ATLCICIIALICESO) Cam Tree re GL eke eee oe ee ee ine wines Chet 405 
Neophasia menapia (Felder & Felder) (Lepidoptera: Pieridae), see pine butterfly 
eet CEVA CUT OTC tat mmr Peta eer as is cee oie a olin aiaty sche tye Riau ae ects hee Soho eek obs eee 454 
Nezara viridula (Linnaeus) (Heteroptera: Pentatomidae), see southern green stink bug 
Nicotiana tabacum Linnaeus (Solanales: Solanaceae), see tobacco 
Bro OU Wie wear acl ev.S tera cr ie wet tee enero de dean te src Wai. e cat, Suyeine ls a kick he eis Eo SEL os vee owe 400 
nightshade, silverleaf, see silverleaf nightshade 
Eo iinem seers SO DCE ecm sa ct eter (Rei mmo Thi 2.5 earn ge oe ee wet SE ass Se ge be faa ss 535 
Noctuidae/noctuid(s) (Lepidoptera) (see also cutworms) .................. 29, 54, 271, 289, 302, 303, 416 
Nomia melanderi Cockerell (Hymenoptera: Halictidae), see alkali bee 
Nomuraea rileyi (Farlow) Samson ({(Class Hyphomycetes] Moniliales)................... 70, 288, 308-310 
ever IGCCIVALUS( CSUN G) V acts retin oer st route, Wiel a tin, ace heielae a dae ee 6 Seren a> 277, 280-282, 317 
eral uN CHEW OL Whee ere te entree ire ict miu ttot hb ay latsieth lat wibG.4 alia e Lielnla oar See ahs & 317, 
Cr uCPLia er CCR Lemme ter CPE erty ot os Eadie ote. JEL wikts VialGN Sid's aikoawh fae Bee oles’ 282 
ES CLIIES COVGNICUSTR et ee te ee Ae 5 Se eee ee ee Cee a ws bees 281 
northern 
CORTE LOOLW OEE) TOL OEIC DOF OCT I Fay Erie nile ute eld oes one wets eostalelels Give volts elas oss Rbléte bls sew bas StF, 
GIN UV eLCibes emer MOMERE VINCIMICH ix, sale 2 a oralse see. sues adisiaale se 8.v ee Ge ee se een ees wt 
SUCH OM me LPO eC CIOCHICNS tern errr. Whar Unt wh Gus ae aa oe oe ee eo Sis Coo a ee es 462 
Norway pine, see red pine 
"Nosema disease" of honey bees, see Nosema apis 
Nosema (Microsporida: Nosematidae) 
CETIG OPH ACUMIICITY Meter e) ree elites dial as ear. CP re teak © he VE EEG A EO Yas cee s vie he es 312 
DICE GEN NTA deel a, eee Va ete tL eA . vere chet iets a waw Sass elke eh oes 158, 284 
gprs canoer, Nosema disease Of honey bees Pe 2s Pi ek a ns 274, 296, 297, 300, 324, 328 
Ce LLC In eee eT Re eer ths er ote ahaa asi "a ataPaterh vain alvlalelaeleiie baa%s Wi lavele ol gte awed « 312 
ier ornidau aOmns Oleh os ett TaN Noe Sa oe yis kk Smarter An ee Awe laces ese oie wate s 115, 452 


heterosporum, = Vairimorpha heterosporum 


615 


locusiae Canning, 195355 ais a «cei ois rg rates a are p enn see 35,.36,,/0, 158, 284, 3125505 


plodiae Kellen & Lindegren «01.4 i053 acti). <r te Saget) ie eel so mee eee nee 2h 
pyrausta (Palliot) (= Perezia pyraustac) 0 fags ei ain on eee dee 34, 124, 140, 291 
seripta (Bauer & Pankratz:1993) 2. nc oe pele octet le oe SR eee a 415 
SPP~ ow dads fs ob BT aad ahs Gall hg, See By eke 6 Wale ee ae a een 112 
as "Thelohania™. I MOSQUITOES « ea Fa I ets aes tate set ene isha eet he eee ee eee 35, 159, 284 
NPV, see nuclear polyhedrosis virus 
Nucifraga columbiana (Wilson) ([Class Aves] Passeriformes: Corvidae) ............ 00.0.0 ese eee eens 536 
nuclear polyhedrosis virus (NPV) (Baculoviridae) ..... 20,31, 35, 364103,.104, 107, 11.1)270-272, 2815282 


288, 289, 291, 299-304, 306-308, 310, 318, 419, 424-427, 429-431, 433, 435-438, 451, 452 
multicapsid/multiply-occluded/multiply embedded/multiply enveloped (MNPV) see multiply occluded 
nuclear polyhedrosis virus 


of alfalfa caterpillar 00. G8 han ccc wine te eects © vos egal a ctiictea thc ned etc ae 20 
Of alfalfa looper. fats nee es othe ee ie oh ai oe CR ie ke ne ee 31,.355,36209, J lye eee 
of. almond moth os. oy oc eda be ee 5 ce 2 pas eee Aten <cupaaleca ies wel ee 300 
of cabbage looper, Trichoplusia ni NPV 7 0. .2 1s ac: chameu deus cioeneaen lS ae) eee 35,318 
of celery looper.) fe. he. oe Cele ea las ce ental oo oe ame eee 72 
of corn earworm (..0 3... soos Gans ete s «as Oe aso 2 6 ic kabaecgaead mene Sea it ee eae oe 35, 36 
of Douglas-fir. tussock:moth, 25). scence oes cha 1a 2 a ee a 102, 103, 113, 288, 435-437 
of European! pine sawily 0) 4.2. aGie. oe cle 8 ae, 4 ge eee oe 20, 104, 438 
OF fall Army woOrnt ence cae ee a sche & uesGie raceeelle oy eG.» 2 tp eae ele meena a ee 35, 288, 289, 300 
of gypsy moth, Lymantria dispar MNPV, LAMNPV, or LdNPV ..... 70-72, 103, 111, 112, 127,303,304) 

306, 307, 419, 424-427 
Of Heliothis (S- lat.) av nS few oo tod SMe &. 5 Slit eceed are eel et Ee ea re ae 36 
of Heliothis/Helicoverpa complex: 25.5... ieeeetac ae ge eee ee er 
of redheaded pine sawfly 507. 2... ted ice ot ees Game oRe nae git a el anna ee ieee ee 116 
OL Spruce DUAWOPM ss) oe eect te oehe cial hee ote Peeae Siete en ae pee Ne 115, 451, 452 
of zebra caterpillar js Soclkparueg Poets ce cia eie hte Hl eres be ease) eon A 300 


singly-embedded (SNPV), see singly-embedded nuclear polyhedrosis virus 

unicapsid, see singly-embedded nuclear polyhedrosis virus 
Nudobius sp. (Coleoptera: Staphylinidae) dts «ye senna cee yee nk es 535 
nutsedge, purple, see purple nutsedge 


O 
Gak(S), (Quercus SOD. cor scr ais ve et epee oe eR ete nC eT tis iar ho ake ee 127, 424, 456, 457 
oak wilt 

Ceratocystis fagacearum 3 icy. 1s bode Anca cee © ae ok a « See ge ee eee ee 457 
Oats, AVENASDD. ma’. okie te tvtele, ce sos see Vine elise ae5 & SRuReminiyS Nukes aueie ts fae ki iret On 121 
Oberea erythrocephala (Schrank) (Coleoptera: Cerambycidae) ............... 0.0 cueeeeeee 85, 124, 141 
occluded ‘VinuSesss oo. ceo we. ace ft + os 5 as) RAMON iia as gen is te ce 282, 301 
Oenopia (Coleoptera: Coccinellidae) 

Congloala (Li) ve sips whe cubes Ce ses ae es Sek ot nate ae ae ee en Re 137 

sauzeti MUISANE.. coh oe Seine took se. een ee ORI ens coe eae an | 454, 538 
Olesicampe benefactor Hinz (Hymenoptera: Ichneumonidae) ............... 00.0 cc cece eee e aces 114, 444 
omnivorous leattier, Cnephasia longand -<sacs.4 ari pt Ae sapien ar ane ne 18, 24 
Onion MASSOL Delia GNUQUA Ts ok aaa etl tee 2 ae eee ee Oi) ee 3292330 
Ooencyrtus (Hymenoptera: Encyrtidae) 

ennomophagus Y OSNUMOtO sic io. «coo +s tens ane cicived came victes chee mec y ane ae 415 

kuvanae (Howard). 36 as «4s eahe Da4 oh os «be dee ne eters, See tee o 422 
Oomyzus incertus (Ratzeburg) (Hymenoptera: Eulophidae) .. 2... .00..2.c8.s04- sees enewcs 30, 122, 138 


Ophiostoma ({Class Pyrenomycetes] Ophiostomatales) 
minus (Hedgc.) Syd. & P. Syd., see bluestain fungus 
multiannulatum (Hedge. & R.W.D. Davidson) ARX, see bluestain fungus 
piliferum (FR.;FR) Syd. & P. Syd., see bluestain fungus 
SD icie bt iagetanttacd eet en ors) < olahiaekaiecccaieh axon Garin aed apeutiinals 2) ceed eee ere a ee a 107, 118, 457 
ulmi (Buisman) Nannf., see Dutch elm disease 
Opiliones, see phalangid(s) 


616 


oan Vee OGY er SOM (Grit a etn Wa Peas vei dee) Gon hae w he dWo ee wld dw ea eaa ewan ees 76 
Opuntia spp. (Caryophyllales: Cactaceae), see pricklypear cacti 

Oracella acuta (Lobdell) (Homoptera: Pseudococcidae), see “loblolly pine mealybug” 

Croius onscurator (Nees) (rymenoptera: Braconidae) ...ccs ccs cece ede Hates tees gmemnseuaae 410 
Orgyia pseudotsugata (McDunnough) (Lepidoptera: Lymantriidae), see Douglas-fir tussock moth 

oriental 


PARE TPO TIECEL UOTE TAT CNIS oe te ee tt ts oc us) ES, Ho chs & MSE Dua vo psc. ape bedh om we’ a biwodvinsle tle ka pas 8 
UIC TY ACH CEI COIS CIS Eten ah ce MR: Wea oid ain RMS ela ye MAM aie eae ee 17, 63, 68, 161, 278 
ee TOOL rn POML INOS 1a wernt Gowen Jukka ed Belen Cg eal WA pAOd se» cue eg 8, 10, 16, 18, 19 
PMU Cee IC OCGMIN OU) CUCECCHS mma Steam, rar at, ide tc) e wag pak Se bay ta tans osible © ah oeaye on as 8,9, 161 
PAG liCa = CHOPS Cen COIS a renter em Em ENT Mer) sek. e ee ivclinhy eats PGbe eb sled, glere wuerdle.e Bvia)cssye os > a2 
EOrMenial Che stnle Dall WASP, e/a OCOSINUS KIM IDITI US’ ide 2 gue dle sis); Su pMl aw As nlats gaye ttya pan sua aa +s 55 
Orrina phyllobius, see Ditylenchus phyllobius 
TE tes ecinvy gyees Sad i aa tou gO RRS eC Se a Pe rk gn 35, 36 


Orobanche ramosa (Scrophulariales: Orobanchaceae), see hemp broomrape 
Oryza sativa L. (Cyperales: Poaceae), see rice 
Osmia lingaria propinqua Cresson (Hymenoptera: Megachilidae), see "blue orchard bee" 
Ostrinia (Lepidoptera: Pyralidae) 
furnacalis (Guenée), see "Asian corn borer" 
nubilalis (Hiibner), see European corn borer 
Otiorhynchus (Coleoptera: Curculionidae) 
ligustici (Linnaeus), see alfalfa snout beetle 


TaR ony Eenug acts BL Ones Stone ha Geet ote Cen ne ene 329-330 
Oulema melanopus (Linnaeus) (Coleoptera: Chrysomelidae), see cereal leaf beetle 
Oucesta ceovrapmica (Fabricius) (Lepidoperas Noctuidae) os... cc. sae aiieatene eas ern dia aie es ¢ sees 85, 141 
(aia ear Guenec) (Lepidoptera: GeOMetiridae). oc nc cc eee ea ees oa oot cee ee ce ine es 111, 416 


Oxyopidae/oxyopid (Araneae), see lynx spiders 


P 

Pachnaeus (Coleoptera: Curculionidae) 
litus (Germar), citrus root weevil, see citrus "root weevil complex" 
opalus (Oliver), see citrus "root weevil complex" 


CTF R 8 cian dagen cg cbse depts cuban: MS PELE AD RE nA ee ane SE ef a ey a ee 68 
Pachycerus eccoptogastri, = Roptrocerus xylophagorum 
Pacific 

hemlock, see western hemlock 

EV POL SOUSA OGL GATES Wie bee A fs, Ayal 2 Oed Sa Ee Re a ger a en earn 454 
Paecilomyces [Class: Hyphomycetes] 

Wire sor Oreeek WiizeyBrO WoC SING te ea ota tain pi eee Sys Nitrs oo 8 tis aie Oe pL oe ee Sins ws 331 

SN er a sO Se alee a Te otis a ee eof Wich alin seis ih 2 06 9 Lob ai at mds pu olla sewn avd 13/ 
Ps beearc pe CI CUt yy Cieactned OF OFES OFTRO OVI A avoir spas bd oun ele gs ea Sac bass. via g ape Bb ani G64, 500.5, ys bscas 317 


Paleacrita (Lepidoptera: Geometridae) 
spp., see cankerworms 
vernata (Peck), see spring cankerworm 


De evOrinia rane Mirae OIDLeTa sh ACHIMIGAC) | 0 aye oe errant av Go Ok kee Pain os bie Senne ett ale ese eds 65 
Palloptera (Diptera: Pallopteridae) 
PAE SELECT ee RLM Myke ale suis Riv a foitia aba irgeiiand oF Fis Fos + “BADIA poe Pia. nace» 401 
parallela = P. modesta 
eamagremimidae (clase secementia) RNADGINa) 5k) wie eo sooo elec ode let A pt otis celle tua 536 
Panagrolaimus dentatus (Thorne) Rtihm ([Class Secernentia] Rhabditida: Panagrolaimidae) ........... 536 
Pandora neoaphidis (Remaudiére & Hennebert) Humber ([Class Zygomycetes] Entomophthorales: 
EemtoniO Di UM ACe ae) meer etme Mama onan Riclad piles «dd Ce 2 Fare SR Bs Rin a takes, dias 330 


Panogrotus obtusa Fuchs, = Parasitorhabditis obtusa 
Panonychus citri (McGregor), see citrus red mite 
Papaver somniferum L. (Papaverales: Papaveraceae), see "opium poppy" 
Parasetigena (Diptera: Tachinidae) 
SAT CAITR ODINC AL CSVOIAY Nita ta tate ys Chel nts ish clea la cath vet ai a ewiere siete ea cas willow the 419, 422 


ara ha P| 
SPP ee cee elas ole ule eteilore e's ple sh phely Wieland o's Mai op cates 1 doettata ae ee a ae ee 
Parasitaphelenchus ({Class Secernentia] Tylenchida: Aphelenchidae) 


acroposthion (Steiner) RUHM 7. 2) s)'..5. 0s ake elke 5 «eee ees eee Ee ee eee 536 

dendroctoni MaSsey on ee ices orale in tgh san ss aon vt kG, Hes Eo Sonal ere deca gee ce ea ee eae 405 

gallagheri (Massey) GOOdEY 2Fi60 oe econ wd, AS onl bia a oie rare eke ge ae pre ote 405 
Parasitorhabditis ({Class Secernentia] Rhabditida: Rhabditidae) 

obtusa (Fuchs) Chitwood & Chitwood 2.55. cy ool sie ects s nat yl cms Kiem ee aire 404, 405 

SPP ove Dray eo wre itahs nie Binks et0k cielo att Omer a sain held iets eee ae ee 405 
Paridae ([Class Aves] Passeriformes) Wy). 00.5. oe es oemieaeccts < orf ehy eet ee mae ee ee can 536 


Parus gambeli Ridgeway ({Class Aves] Passeriformes: Paridae), see mountain chickadee 
Passiflora (Violales: Passifloraceae) 

mollissima, = Passiflora tripartita var. mollissima 

tripartita var. mollissima (Kunth) Holm-Niels. & P. Jorg., see "banana poka" 


Pasteuria (Bacillales: Pasteuriaceaé) . 3 %co ce ate a eee ts ceo eee eee epee ct en a 92 
penetrans Sayre'& Starr 1985 ex Thorne 194070 ee oo ce see ale Ape agate a) ee 13, 92 
Spi ee PR Aa eels ele we bee ne as Haare soe ale bia ati oe Sachets O50 aa tel eae siete 7 aiaae (ee rr 40 
thornei Starr’ & Sayre 1988. oo. cena va eis on re bene 2k tee ee eye 6 ste nie eRe ae te anette 13 
Patasson luna (Girault) (Hymenoptera: Mymaridae) s..06-. ce. ioe ce we eee ee ee 139 
Paxillus involutus (Batsch::Fr) ({Class Basidiomyctes] Agaricales)’ <7)... 0... «te ons re ane ee 414 
pea, Pisum'sativum U: (Fabales: Fabaceae)’. i. 0. S252 Fe es regen ees as a ae 28, 42, 93 
pea 
aphid ZA CVTIMOSIPNOMN DISUIN rice. as oa atten aie era oka eee en ees ae 24, 25, 28, 42, 56, 129, 145, 161 
weevil, Bruchus: PISOPUIN |. Fo ssocn es 5s ace» 2 ees: 4 nies me wis! Shunt ss eels 2 en Re ee {5,17 
peach, Prunus persica Vat. Persica’ cos oi. eu ons Bohne, ees san ee ee eee ee 98 
peach: twig borer, Anarsia lineatella (0 ty es 6 ek ae eae a ee 8 
péanutl Arachis ypogded 2... na bes nations ht Cece tne ee ee en ee 41,92, 96,97, 279 
peanut 
root-knot nematode, Meloidogyne arenarid: wii... aS .. aes eee ee ee ee ee 92 
stem rot: sSclerotiumr rolfsii ToGo sk Seca eee ote oe one oe te Stee Cine etn cor ae ae 41 
pear, Pyrus Sppoe% 3 i essa s boats oe daira get + Wire Ecorse eather so facets) «tala eu ne en yy 
pear psylla,“Gacopsyiia pyricola ee ens ston ce oe ae ees Cre ee ee eee 54, 55, 57, 60 
pecan nut casébearer, Acrobasis nuxvorellas. vas tenis al ieee sites alee eee ee ee 10 
Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), see pink bollworm 
Pediobius foveolatus (Crawford) (Hymenoptera: Eulophidae) .................. 60, 61, 122,127, 138a146 


Peganum harmala L. (Sapindales: Zygophyllaceae), see African rue 
Pegohylemyia seneciella, see "ragwort seed fly" 
Pegomya (Diptera: Anthomyiidae) 


curticornts (Stein): 34 tits P34 hsb hy sare a obs Ce oo he centre ee ee tear ee 141 
euphorbide (Kiellery oS rn ann ee oe a een ea tn Cote enee Perey eee eet ee ee 141 
iFanversaloides Schnabel. visi: 2 Ress ye ave ete wee te ie ee ee 141 
Pelochrista medullana (Staudinger) (Lepidoptera: Tortricidae) ........... 0.0... c cee eee eee 85, 86, 141 
Penicilliay Pentellium sppetics ss S52 % ean ve Oe nlm ole lesen eel an ee me eters eee ere 273 


Penicillium [Class Hyphomycetes] 


corylophilum Dierckx? is calor oie y ve be cs ene ate at ORI eg Sia ae ene ne ee 274 
CFUSTOSENPANOM Ty aide Ve ee oe Pee ne te a ete eneCe Tea es re eee 274 
CXPGNSUAM IDK TSS Os Sa aig Sah Soe Sag MOR Ga oa ce Oe te een rn 98 
Waksmanit Zaleski Wore He eo ed, alee nstencs ethan Uap Saeed eae) ete 329 
spp., see Penicillia 
Pentatomidae/pentatomid (Heteroptera) 2-1 seis cette eer ee tane e ee 434 
peppers Capsicum spp Vide ete tinct «eee Pee ede ete ote tare eon ocean et ee oe 94, 124 
Perezia (Microsporida: Pereziidae) 
dichroplusaé Langer ini eee ae see ava a oe ae ier pet oe ead ee ee 313 
pyraustae Palliot, see Nosema pyraustae 
Peridesmid discus (Walker) (Hymenoptera: Pteromalidaéyr7: 072 7 ee ee 138 
Perillus bioculatus (Fabricius) (Heteroptera: Pentatomidae) |.-—. -.-- a. a eee 139 
Peristenus (Hymenoptera: Braconidae) 
Conrad Marsh Pleat eins se wis cee cb sae ek ve Sev eae Gem pee EET ne nee 59 


618 


Bere GULLS ALAIN EMPIRE Rae EReM I ay eee ys GP Ale. cute Yiannis J «) lets 11514» sh 1g] abs hte ay aoe lage wal Buel als ey 


Reese TONE OSV Nis) ae ene ee te Cec cla set yan: isinava ede es smite sien g mals ¢ sine alt ee © 98 
Petrova (Lepidoptera: Tortricidae) 
Fae Ore CCIE LC ATIT IC 1) MEME tie LMR sty) dass std ise elas acai’ Vel Aas wide baa. Gea sbelcud ace pualaie «6 6 » 412 
So ECO LmI SOMES MM OCS MMPER ROME e ner r te Tectia labs sat soaieg cunts a Zine ot ak ie athe, «a8 Soak p aco ain eon 9! 9) 409 
Dia tanverc obi ial ite tetas PAC ina [ae edn cay Pc guncaunss 09 Pa alc « ake Efi sic auf omied aes ys ae i 446, 448 
Dilanamiieeec (AOU OUIae) Meta En errs Mere seus tec i ace eed sale itis aie «ie We x, velcoa sips h dld'e aed 294 


Phaseolus vulgaris L. (Fabales: Fabaceae), see bean, common, green, or snap 
Phellinus weirii (Murrill) R.L. Gilbertson ({Class Basidiomycetes] Aphyllophorales) 
Phoma medicaginis Malbr. & Roum. in Roum. [Class Coelomycetes], see alfalfa leaf spot 
Phlebia brevispora Nakasone ([Class Basidiomycetes] Aphyllophorales), see whire rot of wood 
Phyllocoptruta oleivora (Ashmead) ([Subclass Acari] Acariformes: Eriophyidae), see citrus rust mite 
Phyllophaga (Coleoptera: Scarabaeidae) 

ERICA UNESCO INT Sa ek SALES I 6 SRN A cS POE ee 414 

spp., see "white grubs" or "June beetles" 
Phymatotrichopsis omnivora (Duggar) Hennebert [Class Hyphomycetes], see Phymatotrichum root rot 
EepyinatOlicnum TOOL TOL? My MOLOIICHODSIS OFMMIVOTG |... 0152 oe cle ya bbe cttw ind sie hag oealéi eee soe 22 
Rr rommi nara WC tassi OMY Ce1es Per ODOSDOLales iim cts hind pine = sets oe 2.6 ats hese btia-> arqeunaie a tun 4 eels 459 

cinnamomi Bands, see littleleaf disease 
Picea (Pinales: Pinaceae) 

glauca (Moench) Voss, see white spruce 

rubens Sarg., see red spruce 

spp., see spruce 
ae et ASE AV OST © ICHLM TINGS) ei tik ee an ek IAN ro. oo hives noes A alin wicge nia af 2 x)4e Ghhs «kb picl eC alone 536 
iP Cie A ONT, ILI SEN eT ETO CTTITELOTE C8 5 eo 4UA ace gh GE MICS Fo PR EOE tai Se le Fa ce mS 54 
Picoides ({Class Aves] Piciformes: Picidae) 

pubescens L., see downy woodpecker 

tridactylus L., see three-toed woodpecker 

villosus L., see hairy woodpecker 


TVICen Wa VARI e eC OLTLAVICIGAC,) Ue enters ASIC tee cd ogn ie si sists alee a4! sve + acmabiie Wy oe icie. 85 lodh teh a okt: ebu 24] 
PIEAY CPt Atl Vy Ol ee rE ee ee cate eee oie sna Cees tan hoe alae ube dial el ya ni wuig) i ge ate a, 

Pieris rapae (Linnaeus) (Lepidoptera: Pieridae), see imported cabbageworm 

BUYER ASSHOP DEL eet DIA cer lann © gant ae A ile Cocina rue n a oee caer els ao a. ahr Gua she sw fiepale, 5406 6) ppd, 312 

lea CIM MII DECK El AL OCODUS DIICOIUS MRIS aie tet cde ne aie GR ENRY ape aifile a sie) no wip a) miei e'le n> igh § 450 

ENCOAe Cia les | em ee eM re epee iin ose errse ete g) sy done Labo ovale 5 Ons 4m Si diee im aids « oc heey 453 

pine(s), Pinus spp........ 104, 107, 117, 399, 400, 406, 407, 410-414, 432, 433, 444, 455, 459, 460, 462-465 


jack, see jack pine 

loblolly, see loblolly pine 
lodgepole, see lodgepole pine 
longleaf, see longleaf pine 
Norway, see red pine 

pinyon, see pinyon pine 
ponderosa, see ponderosa pine 
red, see red pine 

Scotch, see Scotch pine 
shortleaf, see shortleaf pine 
slash, see slash pine 

sugar, see sugar pine 

Virginia, see Virginia pine 
white, see white pine 

western white, see western white pine 


ine 
; LSet eR yeaa EPI Pol 8A el ae heehee TC HEN aN ETC OR Te a 116, 412 
BC OtCT ITO S MEIC ISCOI IIIS SOD Noe nicl eco aig icke We ge fete ta sid ae elie ew eo baie oe ot 421 
ENRP AVE) DS Pi Cee ni aide nee leew actinic alanine bls ee Keane sie shame gos oy ae sins 401, 409 
ECU ie SNe iinet ZCHEr(C HOUIOOCH Rte he tc nis bys eke sys es ne Le tis su 3h sae ee hw eas apes 412 
SRA TTICS eM MRE ete ete crac in isthe 5 alka’ 6140 em kt 8 @ Sie. sie Wie ioe a ehu ia 4 ate Sows 433 


Siskin,-Carduelis Pinus. o ..ciscs reins susc sisyon 2% Poe ORs Weenie due mp ta OM ence yn eee ae 447 

"tip moths," Rhyacionia'spp., see also "shoot borers’ VN vate sae ea shee eee 101, 411 
pineapple mealybug; Dysmicoccus brevipes: 04.0. inh we Paine ead oye he eae eae ae 16 
Pineus pini (Macquart) (Homoptera: Adelgidae), see Eurasian pine adelgid 
pink bollworm, Pectinophora gossypiella (see also cytoplasmic polyhedrosis virus [CPV], and 

iridescent, Virus) Um-1 nett roa 15-18, 24, 36;'68; 70, 72, 125, 270-2,/2,279, 300, 317,319,320 325 

Pinus (Pinales: Pinaceae) 

banksiana Lambert, see jack pine 

contorta Douglas ex Loudon, see lodgepole pine 

echinata Miller, see shortleaf pine 

edulis Engelm., see pinyon pine 

elliottii Engelm., see slash pine 

lambertiana Douglas, see sugar pine 

monticola Douglas ex D. Don, see western white pine 

palustris Miller, see longleaf pine 

ponderosa Douglas ex Lawson, see ponderosa pine 

resinosa Aiton, see red pine 

spp., see pine(s) 

strobus L., see white pine 

sylvestris L., see Scotch pine 

taeda L., see loblolly pine 

virginiana Miller, see Virginia pine 


PINVON Piney PMS CAULIS OR So ope eisai cs cs voringacc bel Aas chy ca ao ras ene ea 404 
‘pinyon piteh module mothy Pe ova GriZOnensiS 5. iv < rune ea toe ee i ae ee 412 
Pisolithus tinctorius (Pers.) Coker & Couch (Pt) ([Class Basidiomycetes] Boletales: 

RATZOPOZONACEE Ji tea mes ncn copnuspode na euens tote epee a pone aadebeoe iam ani een ea 117, 459, 460 


Pissodes strobi (Peck) (Coleoptera: Curculonidae), see Engelmann spruce weevil 
Pistia stratiotes L. (Arales: Araceae), see waterlettuce 


pistol casebéatery Coleophora malivorella a.15 a. he sonic? rere oes ae ee 443 
pitch Canker pF usar tum sUubelulinans yc testy story eer ere eats vey. ee oe 107,117,457 
Pityophthorus (Coleoptera: Scolytidae) 

anneclenis LeConte Pee) BF Sees asd nev cemah selene Pah es oooh erie eee ea ties SAR eae 408 


bisulcatus Eichhoff, see P. annectens 
Plagiodera versicolora Laicharting (Coleoptera: Chrysomelidae), see imported willow leaf beetle 


plant bugs\(Miridae) 225.5 aan ie oe ce ei ee tate ee UN ihe eat ee 26, 29, 42, 52, 54, 56-59, 162 
Plasmodium gallinaceum Brumpt (Haemospororida: Plasmodiidae), see malaria 
Platysoma punctigerum*LeConté (Coleoptera; Histeridac) 7 2.2) (202s ee ee eee 535 


Plecotus townsendii (Miller) (Chiroptera: Vespertilionidae), see Townsend's big-eared bat 
Plodia interpunctella (Hiibner) (Lepidoptera: Pyralidae), see Indianmeal moth 
plumeless thistle" Garauus acanthoides sinter one homer nen ee a 37, 38 
Plutella xylostella (Linnaeus) (Lepidoptera: Plutellidae), see diamondback moth 
Podisus (Heteroptera: Pentatomidae) 
maculiventris (Say see spined soldier bag 22. raters a ee ee 309, 434 
Berieventris UDC: access tes deshale abate 14 emeberenc eve ates Gini a aalles = ioe es eal ee lene vie a 434 
Podosesia syringae (Harris), see lilac borer 
Pogonomyrmex rugosus Emery (Hymenoptera: Formicidae), see rough harvester ant 


poinsettiashuphorbia pul cherrima so coves ket pet ones eet Aedeagal lee 125 
Polistes'spp: (Aymenopterai:V espidac) \) oj ete iin alee Syn ee 29 
polyhedral varies 200 | ARSENAL jects kao rete omaastaeny lea ace pabanragealnc Nn eee nee 432 
"polyhedrosis'virds* of cabbagelooper 25, 0.eacenns patentee ete 31 
Polyporus ([Class' Basidiomycetes] Aphyllophorales) 72.4 .14 ie ata ee ee 459 
ponderosa pines Pinus ponderosa since. se ee eepene nt ee 395, 400, 405, 411, 412 
‘ponderosa pine-tip. moth," Rhyacionia-2ozand)« 22, «aide sei oe ee ee, 110, 412 
Pontania (Lepidoptera: Tenthredinidae) 

sp. nt. pacifica Marlatt. 5. ag tol 2s ie Ore rc ice rtd aa ee Re ee 112, 427 
Popillia japonica Newman (Coleoptera: Scarabaeidae), see Japanese beetle 
Poplar, POPULUS SPP o.iaic: 5 secacirn ach Bsarwhale bi wimiesgete a eee Se: BE PeREeET iene Re aoe ge eee ee 414, 415 


620 


poplar 
leaf rust, see Eurasian poplar leaf rust 
RO ANS DON 1) COS ICC CF A OM UL OF INIT Aa \c (si Jad duotist ain, 08 Ncjovecaivcals ase cel sfatagacedadnya’a's QRRDDN A 107, 117, 457 
OI EL OST ya TS PCL SRA es S Sette Bes EN eee Oe ee ar ee 415 
Populus (Salicales: Salicaceae) 
deltoides Bartram ex Marshall, see cottonwood 
spp., see poplar 
tremuloides Michaux, see trembling aspen 
Poria, see Antrodia 
Portulaca oleracea L. (Caryophyllales: Portulacaceae), see common purslane 


Postia placenta (Fr.) M. Larsen & Lombard ({Class Basidiomycetes] Aphyllophorales) ............... 465 
potato, Solanum tuberosum (see also common scab of potato, and rhizoctonia scurf of 

DRAG aes eee | rT ln, Oa ee oAaTahia Se eles eee wire al 13, 41, 60, 61, 94, 128, 315, 327 
ROU atOMe AN ODOC Eee DOCS Cl IOC wwe Cee OO fg oor, cco hahiy vse felotabeiae a MR MRIS) Aue ER, 56 
powdery scate’disease of honey bees, see also Bacillus pulvifaciens 2.2... ccc ne ck aes ee 274 
pores (enveloped NA viruses: POXViTidac) fence! hae oak en SRR. Rs Jeet 95901 27813,0317 

Be AL SER CULE ORIN unre nee a coi erase aE oop cts, wy 5's) iid Ae alway ahiaPaCSMe\ aisha) al diaeta och ME Seneanala SAT 

MMOL ASSOODEL Se een ee tT Meee te eh rial EOIN Eo olisrara ele scarey < ¥ IQR sare tele S.Ge kewlg S295 13 
Praon gallicum Stary (Hymenoptera: Braconidae: Aphidiinae) ........... 2.0... 0. 138 
Eranyrencnus(|Class secemential lylénchida: Pratylenchidae) <2). 6. a0). ec ce ee ee eee bc eee 59) 
Peeterel ES MVA MATIN IOS CMR Faye ee aii E ene ole opr aciay Sle Son's bn aa eee ASR OMS ALY lee. aD 
BRiCHA ea CACE TO DUI SDI ret Rea etry aiken, olnl's b's si Ges 0 eya'e ns Ye RYDE, ANY YP eae 21, 280 


Prionoxystus robiniae (Peck) (Lepidoptera: Cossidae), see carpenterworm 
Pristiphora erichsonii (Hartig) (Hymenoptera: Tenthredinidae), see larch sawfly 
Propylea quatuordecimpunctata (L.) (Coleoptera: Coccinellidae) ............. 0... e eee eee 129; 137 
Prosopis (Fabales: Fabaceae) 
grandulosa Torr., see honey mesquite 
Juliflora (Sw.) DC., see mesquite 
BaeO20a/ PHOLOZ0All Ge a, et as. heen es aoa a DIAZ IO. 2145 260, 295,31 3M3i e324) 32798282331, 452 
gregarine, (Gregarinida), see gregarine(s) 
microsporidan (Microsporida), see Microsporida 
neogregarine (Neogregarinida), see neogregarine(s) 


pathogen(s) 
Gist Ce ile wee er en eye tet Sd OWEN ECs Lend oT aia Ely BGS a ee o 35 
RHIC OP ber OMS OOSTIIALV ESL POSES: Spar cher, tats ate! 5 clea ors! wait ANAM ARLE Muses SEMI Al eR TE SY 35 
Oia ODeAINCOLE DOI Chante ae mites Ara eee nas oe, ROG ee AR Re. GR 34, 35 
I STINE CP ges oe Bete om, sar inart Sige ESR ae WG Ee a Ree ine Tae a, Sor 286 
ALE CTEM SS a. SB wore cad dor carne 2 nus os Siig TIE a a et eg a a 159, 324 
Olecepidopiera postharvest Pests 4.410 hs See ee Sh ME Ne RIAD IS Pee, . 55 
Ol MOSMMeS Bearer e to t.o 8 oie oL Rae c'e «21s. SR RR Wa. tue TG Lee 85,295 
CEUAVEI Or ANee WOT Maer ee ce eae ors OREO OKI! Bd) ee 276 
CEMItICMiGDECtIES ==, e nereee nas Se eee MRE OES OS wes AREA Ve ely Mat odes, 217 
OE OMNOPLCL rete ee ie ot eR aA Poh REMI es Rd cE ae IES oh 36 


Prunus (Rosales: Rosaceae) 
dulcis (Miller) D.Webb, see almond 
persica (L.) Batsch var. persica, see peach 
Pseudaletia unipuncta (Haworth) (Lepidoptera: Noctuidae), see armyworm 
Pseudaulacaspis pentagona (Targioni-Tozzetti) (Homoptera: Diaspididae), see white peach scale 
Pseudococcidae (Homoptera), see mealybugs 
Pseudococcus (Homoptera: Pseudococcidae) 
boninsus (Kuwana), see gray sugarcane mealybug 
comstocki (Kuwana), see Comstock mealybug 
Pseudohylesinus nebulosus (LeConte) (Coleoptera: Scolytidae), see "Douglas fir pole beetle" 
Pseudomonas ({Class Bacteria, Gram-negative aerobic rods & cocci] Pseudomonadales: 
se RACH OTIC aC cA) MN ttn te Ne VICE Io icin Goa Silidld swria's ew calns SMS woe Salwla ee woe a 95 
aeruginosa (Schroeter 1872) Migula 1900, see septicemia of honey bees 
apiseptica, = P. aeruginosa 


621 


cepacia Janisiewicz (PC 742) 2 e22 eins oe Sus ous s «oo ae tals area ah ee 97, 98 


flourescens Miguila 1895, su 9.2% cisParsiasars aisige ss a e'> = wv + REE nc een et ht ee nee ae a eae 96, 98 
gladioli Sever innd cay ca-0) sree she) testpiep avn) o\ )'elarataned «shor ar sper cndeee dopa Ota RAO Oat a ee ere eer 457 
SPP ico ssiiein «sia, coupe SBR racaneheatepel hahah metal innaha be sheet ger ehahene duet diihe Sete Oe eee mee 118, 456, 457 


Pseudoplusia includens (Walker) (Lepidoptera: Noctuidae), see soybean looper 
Pseudotsuga menziesii (Mirbel) Franco (Pinales: Pinaceae), see Douglas-fir 
Psidium cattleianum Sabine (Myrtales: Myrtaceae), see "strawberry guava" 


Psyttalia fletcheri (Silvestri) (Hymenoptera: Braconidae) ........ 0.60.0. eee cere ete eee teeters serene 63 
Pt, see Pisolithus tinctorius 
Pterolonche inspersa Staudinger (Lepidoptera: Pterolonchidae) ...............0 00 eee eee eee 85, 86, 140 
Pteromalidae/pteromalid(s) (Hymenoptera) 2205 2. waite Seer tsa pitince Ob ale alietere tet hie ee 396, 535 
Pteromalus puparum (Linnaeus) (Hymenoptera: Pteromalidae)= 2229225 Silk SOLE ee eee 65 
Puccinia (Uredinales: Pucciniaceae) 
canaliculata (Schw.) Lagerh.. ssasemawened ae + oes sos once ota. ee es geo 90 
carduorum Jacky. «<0: «asee wala. 5 sn ERIS POE OE, OR Pret meee 88-91 
chondrillina Bubak.& Sydenham. 2.25 3805 ete eo tea Be on © he 84, 88, 91 
Jace Ge, QU ey cess serch aes Wes 6 apt 5 Ry el a uae ain, 0a aR AAT eee 88, 91 
Pullus impexus, = Scymnus impexus 
puncturevine, Tribulus terrestris co. in 21s tie ate he teehee el eee 24, 36-38, 78, 81, 146, 161 
purple 
brood, see subject index 
loosestrife; Lythrum saliéaria woth O56 5 saa ae erod sim diate oes ane ot od ete ee 83, 84, 154, 162 
nutsedge, Cyperus.rotundus .. . 28 DOL PE AIS Oe 81 


purslane, common, see common purslane 
Pyemotes ({Subclass Acari] Acariformes: Pyemotidae) 


barbara:Moser, Smiley & Otvos ..5 $. gj. bases ews oe che fee oe ee 409 
dryas:(Vitzthum) 3. snows apnea oe MAL? RAO De Sines Lee eee ee a 408 
giganticus Cross;.Moser & Rack isis jigs a See oe 5 ec Ce ee cue ee 408 
parviscolyli Cross: So. MoSerinwameid sor wate aie wake etlaons, Sea dies saad alder ek Ae ke 408 
tritici Lagréze-Fossat & Montane .. 0... Jos... paso. s eee ee ae 63 


Pygmephorus bennetti, = Siteroptes bennetti 

"pygmy locust," see pigmy grasshopper 

Pyrenophora tan spot, Pyrenophora trichostoma (Fr. (Fuckel) ({Class Loculoascomycetes] Dothidiales) .... 98 
Pyrenophora trichostoma (Fr. (Fuckel) ([Class Loculoascomycetes] Dothidiales), see Pyrenophora tan spot 
Pyrrhalta luteola, = Xanthogaleruca luteola 

Pyrus spp. (Rosales: Rosaceae), see pear 


Pythidae { Coleoptera) s.3 4 t4.cra'us ote Sia re ea eer Me ao Pipiace a Fee sed ea «ge a 533 
Pythium 

damping-off of cotton, see damping-off of cotton 

toot rot of wheat,.Pythium aphanidermatuimn sas. cus cur aso ter as yes ee ee eee 95 
Pythium ([Class Oomycetes] Peronosporales)i- eae. 525-2 cee ee eee 94, 459 


aphanidermatum (Edson) Fitzp., see Pythium root rot of wheat 

debaryanum Act. non R. Hesse, see damping-off of pine seedlings 

sp..causing root disease «ss. os ee sk ccaGae wos oh ae ea theo «oe oe sgh a eee ee 456 

spp., see damping-off of ornamental plants and of vegetables 

ultimum Trow (see also damping-off of cotton) 
Pytho planus.Herbst (Coleoptera: Pythidac)i@ 09. oukee, ee tla eee ee 535 


Q 

Quadraspidiotus perniciosus (Comstock) (Homoptera: Diaspididae), see San Jose scale 

quaking aspen, see trembling aspen 

Quedius longipennis Mannerheim (Coleoptera: Staphylinidae) .................0.. 00 cece eee e ee ee 532 
Quercus spp. (Fagales: Fagaceae), see oak 


R 
rabbit(s), (Lagomorpha: Leporidae), 5 veeqs o2 Ace eat ae no ee 462 
Rachiplusia ou Guenée (Lepidoptera: Noctuidae) 7720-45. > «© 0 ee . 291 


622 


ragwort, see tansy ragwort 


"ragwort 

Bie OCLC MT OE OILOT S185 CODA C MM iia inlet rida GAA ea Ret AtAR SW ws hogs Sh nse oH oe eves 38, 84 

Seer vaae 0 (QMOD GC SCHCCICIIC. cu A anna «ei Yat ee GER gue ehiondaned Pearcordegeok 38 
Been Ofer FC 1d [LCL emer Fgh pag lil a 12> ae BY aig PANNE SILA vies <dis oS) amore yea y= 279 
Rare atoll dba iCmilened OlVidGm tote seis bag clk. Sabie Pee Sake ahaa! oes eine + « 10 
Ranunculus ficaria L. (Ranunculales: Ranunculaceae), see "lesser celandine" 
red 

Painoltcusile Ont. SOLENOMSISIIVICIA Eo stay nad Gig ass eeee ae ) moptind eo aa Ms ose 285 

OCLEG 2 VALORIS ROT Re MP Rar Meee eS rsh alg iF SE i HGS Ses Fa) od Aeon ast b-eres 285 

Ria Os CET ID ET ae ae ee I aan ew Ss a bog Rade 8 oh x se 6 se ES Byles 415 

Dem ier CIOS ree Pet ee ee ie tang. oly. dg cole. Sune wie deed Shs pce oa 410, 411, 414, 438, 456 

nem ale AA GESSICOCCUS FESIMOS CGN tM Aen ehh tie, wilde 4.f,cic bank AA. SHAG Oe ook 55, 102 

BORICE ICEL UDCI rete te Sanat COE Ne Peis ciaids ooialy Sos 6s 4 este mtingiee dete ne 448 

erenir Gama PEI ES GILT TEU SOVUCHS Ce ees aes wise Melee S009 6 oi eis dil wk ole baie g oma cin ae ca hieys 444, 448 
Pe Drcastea miuthiatcn i SiMLaiCQNOUCHS ISH pany). o. Ad eee Aas El MA ie SE b Sirens Hae 434, 536 
Ream AnCeOneamOuleteAroyr Omen VAINNNONT angen oe oo Sse 6 ee fas che s Sa wee wed Oe weer Ba 30 
PeDCROEC DING SAW LV WN COCIDTION JECOIME! oc Get. Pua Ft aes oes vis SB Say oo PERRO 104, 115 
Reesimermis nielseni = Romanomermis culicivorax 
Regulus satrapa Lichtenstein ([Class Aves] Passeriformes: Muscicapidae), see golden-crowned kinglet 
Retinia (Lepidoptera: Tortricidae) 

metallica Busck, see "metallic pitch nodule moth" 

SE RUESCCEAISO MSOC OOLCTS 1) Ore ee ee i, sie a in ws bans pints 2s GWNRA SETA AER Re 409 
Mabditid nematodes ({Class Secernentia] Rhabditida) ........ 2... 6.2 sce cewtiwe wa sues soled eaves 316, 405 
Rhabditida [Class Secernentia], see rhabditid nematodes 
rhabdovirus-like particles 

BPH SOTO ICK CUE Meme EOI er Mel re ait Ones Se se Feels Gos n> oe NI MOG ERAGE ESS Maas 300 


Rhaconotus roslinensis Lal. (Hymenoptera: Braconidae) ............ 2.0.0.0 cece cece eee eee 128 
Rhagoletis (Diptera: Tephritidae) 

cingulata (Loew), see cherry maggot 

mendax Curran, see blueberry maggot 

pomonella (Walsh), see apple maggot 
Rhinacola forticornis Reuter (Homoptera: Miridae), see western plant bug 


Pr OC tOMia SCUTIL POAC ZOCIONIG,SOIQNL. Je yal. 2.2 « «Sie tans 4B ine WIA ree St 4 eed LE 94 
PR IZOCIOHIC LG lacs A GANOMYCeLeS Mae ona aie sis puis 9S o's» «oan ss ANSE ye EEO 41, 89, 90, 93, 94, 459 
solani Kiihn (see also damping-off of cotton, fruit rot of cucumber, rhizoctonia or black scurf of 
OUAO aie ie  oes hn et eme s na? ole eerie Se wen noite NY aos 94- 96 
sp. 
SaUst Sat OGHUISCASC ar ear ee tate ey Ato ch lua h55 Se MEET II & Sem ORR GSR 456 
spp. 
causing damping-off of ornamental plants, see damping-off of ornamental plants 
causing damping-off of vegetables, see damping-off of vegetables 
Causing leafy spurge stand reduction sn44.5... dos. sn ate eames Had Lia ees eacaaes .9e 89, 90 
as root rot of bean, see root rot of bean 
Bri reste a MAGEE Ge OLCOD ICCA) tay ee ae he acate eae Metac oy iy lle «azo ol mys > POR GMSN- Tea REIN = Js anil 535 
Rhizophagus (Coleoptera: Rhizophagidae) 
TOTTI OS a A Oe SO RST tore COS ae ee eC aan ee eer 107, 108, 395, 396 
Dae Oy ee Oe ice Pe Ae ake alate tedesad spr wah TRCN VANES a0 2 Ada teh ea M a Taw 533 
Rhizopogon ({Class Basidiomycetes] Boletales: Rhizopogonaceae) ........ 2... eee eee eee eee 461 
PRTIPSERIG LORY De ACS MC AIZODUS SOU QT) CFM aaa ce. shove side cdeacdeig 2) i WANs oka ya a CORR aie OY se ss 99 
Rhizopus ({Class Zygomycetes] Mucorales: Mucoraceae) 
nigricans Ehrenb. = R. stolonifer 
stolonifer (Ehrenb.:Fr.) Vuill., see also Rhizopus rot of peaches ......... 06... e eee eee cece eaee 274 
Rhizotrogus majalis (Razoumowsky) (Coleoptera: Scarabaeidae), see European chafer 
Rhodeserass neal yous AMOHING OT AININIS ha cccsine sie ot oe wien as 2 nee ee ce 18, 24, 26, 27, 145, 161 
Rhopalicus pulchripennis (Crawford) (Hymenoptera: Pteromalidae) ................. 0.0. seen eee. Ee 


623 


Rhyacionia (Lepidoptera: Tortricidae) i... © 62625, ow sean ein oor ee el ee ee ee ee 410 
buoliana (Denis & Schiffermiiller), see European pine shoot moth 
bushnelli (Busck), see western pine tip moth 
frustrana (Comstock), see Nantucket pine tip moth 
neomexicana (Dyar), see southwestern pine tip moth 


spp.,see-also "pine tip moths;“»and /“shoot borers icc soma) oers ee oe « ees eee reer 409, 411 
zozana (Kearfott), see "ponderosa pine tip moth" 
rices Oryza sativa 2S edees y Ry Ts PRIS: os 5 sos we > ole ee ees ee 295 
rickettsia.([Class Rickettsiae] Rickettsiales) 2.2. .24/.4¢: esc veut aey Seen eee ere eee 298, 313 
rickettsia-like,»organism(S)¢ x0 2< .. 4s tate es Ce oa SENS as Parkes che Re Re ee eee 3010315; 347 
in. carabid beetles 4.4.4 Jusacseeleee ors Hae GRE KOR BSS PS e eee he eee eee 317 
int Catleasi./by <1, Sowa 4 Paes Sees Re ee Ries Week See ee Se 301 
Rickettsiella (Rickettsiales: Wolbachia€) = ss4500.%% 4.5440 5652552 2 nee eee ent oe eee 36, 276 
from navel.orangeworm> 4 2ys.5.0245 a5 0%55 56 o1as SR ERE Some hee GS ee 276 
RNA: ViTuS(€S)* Qaketin.% 66 pie NS 258 FEEL hee Bb SA te ee Re ree ee 36,276; 277, 2808312 
of cabbage looper; Trichopliusia.ni RNA virus (TRV) «..%:....55 . 0 Pee eee ee ee 280 
IN QFaSShOPPeElS: vce on saw Awa SRA RAGES amare WAG RA Ge we, eM ee eee eee yee 312 
ity navel. orangewormM: che vey Aw Wie Fee ss Sie Ee TE Se wR Re Oe CN RS 276 


Rodolia cardinalis (Mulsant) (Coleoptera: Coccinellidae), see vedalia beetle 
Rogas (Hymenoptera: Braconidae) 
lymantriae, see Aleiodes lymantriae 
Romanomermis culicivorax Ross & Smith 1976, ([Class Adenophorea] Enoplida: Mermithidae) 


(= Reesimermis:nielseni) ty. & 52448 Heres ee ee OE EO ee ee 33, 66, 294 
root-knot nematodes, Meloidogyne SPP iii scien seu cain « Se ee ey ee ee ne, 22791 
root-lesion nematodes,.Pratylenchus spp. eden sees sn Pee ee ee eee 13 


root rot(s) 
annosus, see annosus root rot 
Aphanomyces, see Aphanomyces root rot of peas 
Armillaria, see Armillaria root rot 
of bean, see bean root rot 
black, see black root rot of bean 
of peas, see Aphanomyces root rot of peas 
Of PINES csi ngedinds weraiciae siehete RA FE ye 2a Ear a Wy ee iS 
Phymatotrichium, see Phymatotrichium root rot 
Pythium, see Pythium root rot of wheat 
of wheat, see Pythium root rot of wheat 


Roptrocerus xylophagorum (Ratzeburg) (Hymenoptera: Pteromalidae) .....................0.0000 ee 325 
rough 
harvester. ant, Pogonomyrmex, rugosus: ah cda eats cs toes caclsneieo eee ees 275 
lemon; Citrus jambhiriscecsgshtestalas tees oe oie aes 3, aod we apeeiaa ee  ee 127 
roundheaded pine beetle sDendroctonus adjunctus 204m, 2". SS ne ee 405 


rubberweed, bitter, see bitter rubberweed 
Rubus spp. (Rosales: Rosaceae), see blackberry 
Rumex crispus L. (Polygonales: Polygonaceae), see curly dock 


rush skeletonweed, Chondrilla juncea galaxy age eta ee, Se eee 76-78, 84, 88, 90 
Russian 
knapweed, Acroptilon. repens ne ag Woks 2 ede ao ee 76, 79, 84, 90 
thistle, Salsola australis (Ss iberiéa) Wan naeeee ee eee 37, 78, 82 
wheat aphid (RWA), Diuraphis noxia. ; 7726 ee 54, 58, 124, 129, 137, 148, 330, 331 
Russian-olive, Elaeagnusiangustifolia ju5-34.03 were. eeeee as ee ee 82 
rust(s) 


on bean, see bean rust 
Cronartium, see Cronartium rusts 
fusiform, see fusiform rust 

rye, Secale cereale 


624 


S 
Ree ORICICRORIIONE DCE S MAO TTON CELOIIUS Poe PS at 6 au 2.6 3's RA Es 9 ES ENG 296 
Saccharum officinarum L. (Cyperales: Poaceae), see sugarcane 
Saissetia spp., see black scales 
Salix (Salicales: Salicaceae) 
lasiolepis Benth., see "arroyo willow" 
spp., see willow 
Salsola (Caryophyllales: Chenopodiaceae) 
australis R. Br., see Russian thistle 
iberica Sennen & Pau, see S. australis 


PIC CAL eI ON LED MAMMOSIS SING Wine EN aks 2 oc untsesvsh cialis Soalardis se A Pe > Dee 76, 82, 86, 154 
Salticidae (Araneae), see jumping spiders 

MAMI ARS TICALCID LAL Lisi] OMCNO ACh CU nian et tue cc Rees 5 Ae «AGE TH, Se ee OG 6S 29, 31 
Salvia aethiopis L. (Lamiales: Lamiaceae), see Mediterranean sage 

Brain OSOISCAIE HE CICS TIA OLUSADEPINCIOSUS iiiiin, ch css dens: S,deto sacs porepar OO OOM A Net MS AOD. Ae V7 TS 
SansucKers ((C1asseA ves|ir iclionmes: Picidae imnmsnie seantiniast ae Sake Si hte obitesl sc ewe. 396 
Sarcophagidae (Diptera), see flies, flesh 

SALTON CIDR TIC LOITGISTLITC ES MME COMET rn RS hha rele AN RAS eae DOL Wack hen WEAN Wa 7, 8,9, 161 


sawflies (Hymenoptera: Cephidae, Diprionidae, Tenthredinidae) (see also "birch leafmining 
sawfly," blackheaded pine sawfly, European pine sawfly, European spruce sawfly, European 
wheat stem sawfly, introduced pine sawfly, larch sawfly, redheaded pine sawfly, Virginia pine 
sawfly, Swaine jack pine sawfly, wheat stem sawfly, Pontania sp., and nuclear polyhedrosis 


SURES AEDST Es bp meee PRON PORNO ge a cls, nobchctatay' at of cx aicosc cals SRC Pee ay alga, TINY 101, 102, 427, 432, 433 
SeAlesmomoprerassupemamily COccoidea) ya aamee. cei baaer ts oma ike TQ ALN BORQO SS RSIS 62 
SimMaOrecASHIGIGAS ie wae el Hee eet Re cay Se tis Das c eee Ea eee Sosy UE, 91555356 
Pe aisPeT EO LASPIGICLAC) ae tase an Pe Sealy us Id lM EM Peed SEA. AR BES 5D 
Sc arapemtO COicra a Scarabaeidae): tease oe ae aes tad eens aes AML Seay Pee Seam 412,414 


Scarabaeidae/scarabaeid (Coleoptera), see beetles, "dung," or beetles, scarabaeid 
Schizaphis graminum (Rondani) (Homoptera: Aphididae), see greenbug 


Schizosthetus lyriformis (McGraw & Farrier) ({Subclass Acari] Parasitiformes: Macrochelidae) ......... 406 
Sciaridae (Diptera), see darkwinged fungus gnats 
EP rriH| @ LASsaPISCOMVCEIES | (HICIOUAIES ) ane oy lak et ee nia oe ss oa Vets SN 93 
Sclerotium blight 
LDA Se] CFOs COL Sil men a ie ey Lee eek ee es Sees) OTE eee 94 
CVEg pre AINE SIC? OLIGO Lf SII Gee hared re ee aint 2s dyes, God) shalcn tm) a Oats Sey A I LET Wd 80 Woe Pe are a 93 
CIEL OMI AL CAASST 1 DOUCINY COLES | 1.7. er oes ors Gos «2h SR ee, SAR oT 94, 459 
rolfsii Sacc., see peanut stem rot, and Sclerotium blight of bean and peanut 
CalisinmaiseasesrO  fOimlalO and PeEPPel a gat ks shew ee nde Me Pee Seta Nate A 94 
Scolytidae, see beetles, bark 
Scolytus (Coleoptera: Scolytidae) 
multistriatus (Marsham), see smaller European elm bark beetle 
ventralis LeConte, see fir engraver 
Scotch 
PEE VISES SCODUPIUSL os do ates shdn ob vise Wade vine Sa eR Es VE EMIS ee og ORAS ee 36, 37, 78 
PIRES Ey POSTER ors, PAR win 62S. 218 Sta Lie yates ne a IND OOD FES TEE 411 
Scymnus (Coleoptera: Coccinellidae) 
FBGA ENE), 3 ap GaN. asa yeyee tr Bini Rg e238 da ata ea A a ee 1298157 
PINEKUS A VUISANG Ee re ae seed wate oe ety alee CAMS AE ene A gee one GM Ne Say. 454, 537-539 
URI CA NGCISE ) PRM, Hor ee ate es One 2 elas Neem aiereieielee ee aibicns aie sai a's Salale Syme wees Shs 538,539 
ee aioe lacs ty PHOmyCctes || -e maa ae cage Cae tad 2s cael Sets ey eae AUG SS. 465 
Tce rol eehante ens Seen eit Cee re els wig cle Sia dale a pe EMS ae, 465 
“red ico ak uninat Carmichael dé. Millen toa) sean is oh Gude ta ad. MOR NSS OM ee. 456 
Secale cereale L. (Cyperales: Poaceae), see rye 
Reema oD GRC OTIS Oy UIINOS irate Me Man Ono ie x ad a aig vii vss SEO Rian ns, WR Ee 81, 82 
Semiadalia undecimnotata (Schneider) (Coleoptera: Coccinellidae) .............. 0.00 cece eee eee 137 


Senecio jacobaea L. (Asterales: Asteraceae), see tansy ragwort 
senna, coffee, see coffee senna 


625 


septicemia of honey bees, Pseudomonas aeruginosa. 0. oo. 3c sete oh a ee 297 
Septogloeum gillii Ellis, = Cylindrocarpon gillii 
Septoria leaf blotch of wheat, Septoria tritici. 2s metsaeh. Pak hee a Stes EE ee er 98 
Septoria ({Form-Class Deuteromycotina, Form-Subclass Coelomycetes] Form-Order Sphaeropsidales) 
musiva Peck, anamorph of Mycosphaerella populorum, see poplar leaf spot 
tritici Roberge in Desmaz., see Septoria leaf blotch of wheat 
sesbania, see hemp sesbania 
Sesbania exaltata (Raf.) Rydb. ex A.W. Hill (Fabales: Fabaceae), see hemp sesbania 
Sesiidae/sesiid (Lepidoptera), see clearwing moths 


sevenspotted lady beetle (C7), Coccinella septempunctala ........ 2 aes 1. tee ees ee 124, 129, 137 
sheathminers? Zelleria and Taniva spp. x< sca: sirens es axteestoenside-usnaucuaetoe ote cue) ove eas See ee 409 
shoot anthracnose of dwarf mistletoe; Septogloeum gillii 7.2.2... « Sine ae ee 466 
“shoot borers,” Rhyacionia spp., Retinia'spp., and Petrova spp- 2...2.25. sess ae 409-412 
shortleaf pine; Pinus‘echinata as ..03s5.. « I A ee eee 405, 407 
showy crotalaria, Crotalaria spectabilis. 0.24.5 is cyscscacne = ches «toes HRP en ee 91 
Sialia currucoides (Bechstein) ([Class Aves] Passeriformes: Muscicapidae) ...................-0008. 536 
Siberian elm; Ulmus pumila’. oo. s80. 230 cue Sn) oa odd Se Oa ia Se te te ae re 427 
Sieklepod "Cassia ODIUSIfOLI si. foc3 2 suse WS ED Aya eee ed ERD AA Aa hk 89, 91 


sida, see prickly sida 
Sida spinosa L. (Malvales: Malvaceae), see prickly sida 


silkworm, Bombyx mort YS x GR SS ee EL ET ee Pee. eee 432, 450 
silver fir, Abies alb@iswtet TR. da Sa I a eee eee 453, 454 
silverléaf nightshade Solanum elacagni/olium Vn.4.0n a ee ee ee 123, 128, 141 


Silybum marianum (L.) Gaertn. (Asterales: Asteraceae), see thistle, milk 
Simultidae (Diptera), see flies, black 


Simyra dentinosa Freyer (Lepidoptera? Noctuidae)! . 3... 4.0.0. -« 1 .)) sas 2 ee 85, 141 
singly-embedded nuclear polyhedrosis virus (SNPV) ........... 281, 282, 288, 289, 300, 302, 309-311, 319 
of cabbage looper, Trichoplusia'ni SNPV for TnSNPViy, Ne Ge 2 ee eee 281, 282 
of corm earworm; Helicoverpa zea, HZSNPVe- wan AS ee 302, 310, 311 
of Douglas-firitissock moth’ wanes sgh) ee Se, Pe eg 435 
of Helicoverpa/Heliothisor HZSNPV . 2.5.2 30a 5. 2 ee Oe ee ee 310 
“Heliothis SNPVivas oes 28 ois wesc ate tain) am CAE oA oe ee ee eee 288, 289, 309, 319 


Siteroptes bennetti (Cross & Moser)» 5: ssc 443 ets nes sles es Feed eo ee ogee ee 406 
Sitobion avenae (Fabricius) (Homoptera: Aphididae), see English grain aphid 
Sitona (Coleoptera: Curculionidae) 
cylindricollis Fahraeus, see sweetclover weevil 
SPP Phe Pale Sa Sa ais One ATE AMEE te taeT ERE ae Nee ese Oe 54, 56, 329, 330 
Sitophilus spp., see "grain weevils" 
Sitotroga cerealella (Olivier) (Lepidoptera: Gelechiidae), see Angoumois grain moth 
Sitta ({Class Aves] Passeriformes: Sittidae) 
carolinensis Latham 
canadensis L., see red-breasted nuthatch 


PYSMaea NigOrs Ve PRE Te Pe AOE Oise aie Mee ea TateR tia Re dane ema ee ee 536 


Sittidae ([Class' Aves] Passeriformes)) 52% 29.2225 S27 are oc enema eo 52a ee ee, 536 
skeletonweed, see rush skeletonweed 

slash pine, Pintis elliottii <asu aces ota OSs ose San de ee eee eee 117, 395, 457 
slenderflower thistle; Carduus'tenuiflorus. 12.0. {ia2ca0s 05-2 oe oes ee 37 
slow bee paralysis virus, see chronic bee paralysis virus 

smaller European elm bark beetle, Scolytus multistriatus ..............0.0000. 24, 101, 102, 109, 401, 402 
smallflower galinsoga, Galinsoga parviflora ..... «2. +s5. 4.40025 dene ue ee ee 77, 83 
smooth bedstraw, Galium mollugo:.. «i. s.7 ood was eaaen eee ere es ae ee ee ee 76, 83 
snakeweed(S); Guilerrézia Spp. 0 i... os ssi <'s s on ene, hon Oe ee 77, 81, 82, 86 


broom, see broom snakeweed 

threadleaf, see threadleaf snakeweed 
Solanum (Solanales: Solanaceae) 

elaeagnifolium Cav. 

melongena L., see eggplant 


626 


tuberosum L., see potato 
viarum Dunal, see tropical soda apple 
Solenopsis (Hymenoptera: Formicidae) 
geminata (Fabricius), see fire ant 
invicta Buren, red imported fire ant 
richteri Forel, see black imported fire ant 
spp., see "imported fire ants” 
SEM OUTED OCT OUST T SOE) em tents a Ao eee Atm AMOS ttn 5 0 Bara clk phe sis om a/b wr a elie: w ah RRR NAGINB. 9iGie ols 124 
grain, see grain sorghum 
Sorghum (Cyperales: Poaceae) 
bicolor (L.) Moench, see grain sorghum 
spp., see sorghum 


southern 
corn rootworm, Diabrotica undecimpunctata howardi (see also spotted cucumber beetle) ....... oP leeds 17 
cottonwood, see cottonwood 
ST CCCISCINK MUTE tN Ear VI Tl Aerie AP ee Sea Wed Ron wy Sle us Re al oR 945550574330 
house mosquito, Culex quinquefasciatus (as Culex pipiens fatigans) .........0.6. 00 cece eee 294, 295 
pine beetle: Denarocionus /Tontalistra. ono pi es hee ons 3s 102-105, 109, 395, 402-404, 406-409, 433 
SOMiMvestece Dine UP MOU TA/VACIONIC RCOMECXICONO |. 6 cdysnk os os GA) © ons on 4 2 RRA 411, 412 
Seay ie AM Ca ie aia mae Oe eee on Rls dite asin eo a Fae alee.) SEMOE oA 32754500, 230241274309 
soybean 
By EST AIOUCN Cle OOCTO QV CIES ae ae A ete es ie Pa oS ee havo eK ee ec ME PN a the 92 
MNCL CLG ES CU ICIUCCTIS Me nee RE res i bhi Ee dati cares o's SARUM A SAM Sa) wee 54 
Poona endius Walker (Hymenoptera Pteromalidac) °F: 2.25... ci. cet sk oss ss es SREB Siem en 64 
Spanagonicus albofasciatus (Reuter) (Homoptera: Miridae), see whitemarked plant bug 
Spathius benefactor Matthews (Hymenoptera: Braconidae) 
Sphaerellopsis filum (Biv.-Bern. ex Fr.) Sutton [Class Coelomycetes] .............. 0.0.0 c eee aes 456 
ee Op norme SCLIpio (i) (Li pteta nS YI PHIdae ake fat aaa ¢. 1 Se een) eras em ea... cnadedeide 138 
SAS TOYS NETS TOECe a5, etic chai ayitvaece 4h arlene Ree aR at ae oe ec gee er 536 
Sphaerulariopsis ({Class Secernentia] Tylenchida: Sphaerulariidae) 
DENULOCIORINIASSeY) NICKEL Te tn ren nO = ee eee eo A ele AOE. Ci Wma ewig 404 
USFORAC RC all NICK IC Sete ae, eee eee tine: Fe a Se. year secon. SEOs Hage Wj wats 536 
Sphenoptera jugoslavica Obenberger (Coleoptera: Buprestidae) ................ 0.0 eee eee eee 85, 140 
spiders (1 Cliss Arachnida) Araneida) (2 secs Gcesiaw hie ns eee 116, 310, 411-413, 434, 435, 446, 448, 450 
crab, see crab spiders 
jumping, see jumping spiders 
lynx, see lynx spiders 
Rie SO IIel DUS OGISUS TNACUMVENOTES . cgc.0 ct leusyn tu aunuriontioiegrselsgnieie\naurl ania.» LOI SPERORD EL CBE. 309, 434 
Bpirociicte,s) (class Bacterial spirocheactales)Mangnte tats tamer. ami) Sore al eam inaletn ss 305 
Spiroplasma kunkelli Whitcomb, Chen, Williamson, Liao, & Clark ([Class Mollicutes] Mycoplasmatales: 
Spiroplasmataceae), see corn stunt spiroplasma 
spiroplasma(s), ([Class Mollicutes] Mycoplasmatales: Spiroplasmataceae) ....... 69, 159, 298, 303, 305, 306 
AUST UC Sear ete nee Pitan. re re artee ae ee ae Ope MO ete a A. [heeled ocala dled aan cig BPSas 305 
CiLT (Ls ee Pre eA toy era) oc fees.) eM oe TE Re NEI AS ROTA cite Se 2S4 Me 305 
MeO OTAUO POEALC Dect ever eret rite tots a ete ee So ARR RAINE: SAAS Set PS Std whe 303, 305 
corn stunt, see corn stunt spiroplasma 
Drosophila, see Drosophila sex-ratio spiroplasma 
RRR De Geer ere eee De eee esas A Lap oa eis aia LON, My ROR hays Hs 298, 305 
suckling mouse cataract, see suckling mouse cataract spiroplasma 
Le en ae od Oe ORRIN SH AWS det 9.0 alam kek 2S 305, 306 
Spiroplasmataceae ([Class Mollicutes] Mycoplasmatales) ...............20. cet eee eee eens eee cees 305 
ooaepicra (Lepicoptera. NOCUIGAC)i teat aa weiter iaclag’s a. -i1tere aa ss fem. ods eeneals 6 oi: 54, 67, 68, 272 
exigua (Hiibner), see beet armyworm 
frugiperda (J.E. Smith), see fall armyworm 
ornithogalli (Guenée), see yellowstriped armyworm 
Sporidesmium sclerotivorum Uecker et al. [Class Hyphomycetes] ...............- 000.20 c eee eee. 93 


627 


spotted 


alfalfa aphid, Therioaphis maculata gicaion «.)... e622 ean ee eee 24, 25, 28, 29, 70, 161, 314 

cucumber beetle, Diabrotica undecimpunctata howardi, see also southern corn rootworm 

knapweed,,Centaurea maculosa tj. sey annie ew elals ae ee 76, 84, 85, 123, 140 
"spotted cutworm," Xestia c-nigrum (= Amathes c-nigrum) ...... 006. e cc eee eee eee ees S27 
spring cankerworm, Paleacrita vernatas, 2ij. sue eae + ies Want lc eine, ee LNE RE te nn Mee el veer nae 112, 427 
spruce, Picea Spp a. ciusawiae oso s eb ee ane Bee Pi pieces Sea ee eee 412, 444, 447-450, 453 


red, see red spruce 
white, see white spruce 


spruce 
beetle, Dendroctonus rufipenniSm 25 aes acc © 2 hue) ie ee 101, 102, 108, 395-397, 404 
budworm, Choristoneura fumijerdna wae? ane eee ee ee eae 102-105, 115, 314, 430, 444-453 
“budwormsM. Choristoneura SpDiac. aris tee whe ow SR a oh ee 101-105, 107, 115, 428 
weevil, see Engelmann spruce weevil 

spurge(s), Euphorbia Sppip ioactishaedd a nal. @ ata ase aes ace = Pas al oe ot aia ODS Ct a 78, 79, 83, 84 


cypress, see cypress spurge 
leafy, see leafy spurge 
Spurgia (Diptera: Cecidomyiidae) 


Capitigena (Breml) « 6-06.03 6.5% 5 Shs Sow 0h 0a wo re 6 NR AERO N CNS ONEE aU SNC gt teat Oe ee eee 14] 
estlad GARE: A, lo dtiee Ne ie Rs eee OS Son ede sy ae ated ue ee ee 85, 124, 141 
squarrose. knapweed,. Centaurea virgata Vals SQUATTOSA ~ 25 sche 1s ime +e vets 2 wee) hades ee 1935 
squash,.Cucurbita spp sch s 00. tm wins. oe Soe me Agel yon Wis om OAM ope =) 5b UMP pene ep ee hes 


squirrels (Rodentia: Sciuridae) 
red, see red squirrel 
St. Johnswort, see common St. Johnswort 


stable. fly; Stomoxys calcitrans (2ccctenew . siete ds aise « 2 Mee en A ee ees A 321 
stalk borers, (Lepidoptera: Noctuidae.and/or Pyralidac).2 2)... 2s a ne ee 26 
Staphylinidae (Coleoptera), see also beetles; rovere. Vee... Ae eee. eee eek ee 535 
starthistles, Ceniaured spp accede Poe eRe sn ee See eke bee eke een Cee ee en 89 
Steinernema ([Class Secernentia] Rhabditida: Steinernematidae) ............... 0.00... cece eee eee 67, 68 
carpocapsae (Weiser:1955)\pee ernie vas te 33, 277-279, 307, 316, 317, 327, 405, 409, 412, 452 
feltiae (Filipjev 1934), some records actually S. carpocapsae, see also ........... 68, 139; 27833073327 
glaseri (Stemer 1929) 2c suatentins «vienna eile CERES ee Ak Re, Rk 19, 20 
riobravis. Cabanillas; Poinar &)Raulston1994) 225 .co..4 2.5 ae ca tet le eee 68 
steinernematid nematodes mises =n eres a Aeros ce es ee ee 68, 278, 287, 316, 317, 409 
Steinernematidae ([Class Secernentia] Rhabditida), see steinernematid nematodes 
stemborers, graminaceous (Lepidoptera: Noctuidae and Pyralidae) ............... 0.000 cece ee eee ee 57 
Stilbella [Class Hyphomrycetes] o--i.5e..:502) sai ascot eavcretiets anctane ath eames <e 94 
Stomoxys calcitrans (Linnaeus) (Diptera: Muscidae), see stable fly 
“strawberry: quava;:Psidium cattleianum © 3. )..ahe.s oe oe 5. has Te A Se. a 466 
strawberry: leafroller, Ancylis comptana |. 3.63. save. 4 ahs o SA et ee ee 17, 19 
Streptococcus pluton White (= Melissococcus pluton), see European foulbrood 
Streptomyces ([Class Bacteria] Actinomycetales: Streptomycetaceae) ................ 0.0.0. e ce eee 457 
cacaoi var. asoensis Isono, Nagatsu, Kawashima & Suzuki ............. 000.0 cece cence eee ees 463 
scabies Thaxter, see common scab of potato 
SDD ies POWER «BRIS oo Fn ee wagons see hao ee ney eee ae ne 105, 117, 118, 457 
Striga asiatica (L.) Ktze. (Scrophulariales: Scrophulariaceae), see witchweed 
“striped pine.scale,” J aumeyella pink: tashnies Sots SPO ee ak ed 116, 455 
Strix occidentalis (Xantus de Vesey) ({[Class Aves] Strigiformes: Strigidae), see northern spotted owl 
stunt disease of corn, see corn stunt spiroplasma 
subalpine: fir, Abies lasiocarpa Asehie 3 dca! vm oss a ps eR ene oe ot, le eee Heed ee 454 
Subanguina picridis Brzeski ([Class Secernentia] Tylenchida: Anguinidae)........................05. 79 
suckling mouse:cataract spiroplasma: =... 2.5.2. )2.05 02 + ac an 2+ <> se ene tenn en ane a 305, 306 
sugar pine, Pinus lambertiana® ci. eee 08 hos «nae Pode: Co ee, oe ee 399 
sugarbeet 
nematode/beet cyst nematode/beet eelworm, Heterodera schachtii .........00. 00 cc ccc cece 13 
wireworm, Limoniuscalifornicus 02). 9 pole n's,6 See ee ere ae. ee ee en ee 68, 327 


628 


AERTS 9 lel TEM ENO TECGHTTOIT Cc occclhs Mii 6 oP eae EO age en ce oe 61 
BU ARCANE DOTEERIOIGIFUER SACCHOT IIS var 6 x5 0 tus soow ana hace «0 » RRMA low 7-9, 16, 17, 26, 29, 54, 61, 128 
"sugarcane mealybug," see gray sugarcane mealybug 

"sugarcane rootstock borer weevil," Diaprepes abbreviatus, see citrus "root weevil complex" 

Sulphuretylenchus ([Class Secernentia] Tylenchida: Allantonematidae) 


BI GPOOTUSIMNIASSES \ENICK ICL Gti kOe etd ey oeia spb cuisink ee Gor od > oda + 4aNhn RS 405 

scrutillus (Massey) Nickle = Neoparasitylenchus scrutillus 

enous (Massey) NICK Cates). ahem ee A. Liven sets 208), 21).0..< alah. ta SMS Sarde 405 
SURE T re) LULU Sc CFIPILIIES rote cl nn iets wis, SENN es lk. a Ad SUR ad Pee ough 89 
VATION ACK DIE SAW LLY MINCOGIPTION SWOINEL.. ait wie << Sain id 6 si nieve ws ee GAM Usage Hees ee 104 
RRC CUG ION CLAV CEM IIR LONG CVI INGTICONIN Mitel faa Soc sine X ax Gon «> 2 oe ais RN OE sO ee 18, 24, 25 
SCOTS UIT) SOIC OI CIRSLUICH IE wana Nera ane Se «<5 an, 5) AM RG SEA NE TROLS HOR 5k EMMOTT hte Sgt 460 
VE LOCALLY LEN ITIICIE (1 ELCIL OVS ete cveSeeniiy hk Ser wiles Gey k's'cie' sn) Foe RRA ETRE ae: MME. Sey Ae Pe Lh pg 316 
sweetpotato 

Vee VALE AS Ori COFIUS Cl CCOMUIUS © LA ERE 6 ot Gin se 2ab S655 EO 4ENRTS Baa Va waa SS 72, 316 

BM ALG LC BEL CITI NUCE A OCCT A Rte Nid erence a) a rr scan ace laren 3 MR SY oom 345975 880212 513081372331 


Syngrapha falcifera (= Anagrapha falcifera), see celery looper 


Db niamonaconvzoniara Ls)(Coleopteras@occinellidacy yr Pa. ooo et eee eee eee: 539 

SS roniciae: (SMe tial ieee eat Mee ied Sea Gah eis Enaritaed/Rie eo «(ae ae ee see cl ccs cd es ots 538 

T 

Tabanidae (Diptera), see flies, horse 

Tachinidae/tachinid(s) (Diptera), see flies, tachinid 

take-all disease of wheat, Gaeumannomyces graminis Vat. tritici ..... 6... cc eee 13, 22, 41, 94-96 

Moagrcact |G tases Evrenomycetes | PMroudles) ance ota. clon a. gi oes ehh hav gs en a ee 93 
Eines MRVETE REIN a rence rene 5. son colin. a i eae PRR ea sc a 93 

ARC EIT ATIC IFSC a Oe Tne ee ed feiss ae Sunny ens wa “Supe acute GG 1b dm Blas ao 439, 440 


Tamarix (Violales: Tamaricaceae) 
ramosissima Ledeb., see saltcedar 


Tamiasciurus hudsonicus (Erxleben) ({Class Mammalia] Rodentia: Sciuridae), see red squirrel 
Taniva spp., (Lepidoptera: Torticidae), see "needleminers" 


RAIS VaR OE WOU OM SENECIO [ACO DIC or. Geessed sie. eto phic ae wa = pig spuds in * aim laae 9.9 800 ley oa 36-39, 76, 78, 83, 146, 161 
BEAT MEST OTE CTSA COP LL MMO te na Aero YO St chlo Insel ese At 2 of Mone vals cea asst taK nanscohe Mo aj Sosy; aly 81 
iAP eraGeca Ue A VIUTa Al ITAA Vee bg, See a Moe nclee < aidy oe bao kun scoot S-qirngaa Sa A aha lsnhely a sulepeubnn 21, 40 
PARSON ani DUIS Shy O1Ss 700) Orisa te ae See ce wt Aik hci WSC ae 58 ae ahs mig Caran aiohe “apicy? 42,59 
Tarsonemoides spp. ({Subclass Acari] Acariformes: Tarsonemidae) ............ 2.0... ce eee ee eee eee 409 
Telenomus (Hymenoptera: Scelionidae) 
ELSOD UOC ACLOCK) Uti set NR BEES ook cshsten nia elalas oom iaia ly tiiAtoe ailehs <capeicn x apy a-ane Pag Aare 111, 415, 416 
CEU OFI ICUS ASRINCAC Bet) we ht Rite A Boke cacy: Morir tal ahaa GE sop « 6 ain ayhhatkinslin, wceithve 113, 433, 434 
GSR TANT eA NE TRS Oa aida rd ste TOR PONT TRE ee CT Se ee ee 415 
CEES IO ee ears nk Cystine et neces Crean ag one Bin tae slave stasis! one. 4 oes duets ot wages 65 
Temnochila virescens var. chlorodia Mannerheim (Coleoptera: Trogossitidae) ....................-. 535 
ie aOR HTICIACU Le OLE ODUCT) Mies ee On ts aye ent rit ie tae Eat See Na ahaa cline > ain aslugnrahsl>. whisejesdie ey 535 
Beer LOSE LIVASIOT |e eee ca Rit ate ee eh a) netting AN ap namamistan Wyre diem Wain cuarBile sey 305 
Sent nr eciniciMemua Vy OMCIODLCLA jar tec inet sts 8 eit e acct ips evans Atelical n+ © Byain ec holilin ln, ME MANin vita uxiv 427, 444 
Tephritidae (Diptera), see flies, fruit 
Pera OS er rrciMie PASS AY DUMMYCCLES |p ree oa cote cts) s Soya 5 binds s/o w Se wy B60 A\Sierae oo 0nd Glee 93 
LETS VETOED LG, TT RM ANG FTES ES IR SENS OPE PSE eae ge eRe Oe ee tee 93 
Ter OG VITCHS OC Wel MAIIVLCTA aE COUTINGAG) ty ei cn cea cg NH sas ie fan ths Ws, iin, ease a Ryn ey HS, Hyde 0d 86, 140 
Ret ANIL Sot LSOD LOLS me arse ay Ser og ce go aS ao oh ge SIS lo. datan Sage ch snc 147 
Tetradonema solenopsis Nickle & Jouvenaz ({Class Adenophorea] Enoplida: Tetradonematidae) .... 286, 287 
tetrahymenine ciliate ([Class Oligohymnophorea] Hymenostomatida [Suborder Tetrahymenina]) ........ 281 
Tetranychidae ([Subclass Acari] Acariformes), see mites, spider 
Teruppier ssp OU spp a Lever Opel a. AUMIOCOMIOAC) ai nee nn ne «pis eed eeleine ree wns « 454, 538, 539 


Tetrastichus (Hymenoptera: Eulophidae) 
incertus, see Oomyzus incertus 


629 


julis (Walker) gos c2 225040005 5 oe U RE eG be toe ha 28 te Re car eee eee nee 140 
Tetrigidae (Orthoptera), see pigmy grasshopper 


"Texas broomweed,” Gutierrezia texan ais uo oats ein als Sale es ae ghetto see eete tte veneer 81 
Texas whitebrush, Aloysia gratissima 1... 6.00 ccc eee eee eee eee eee teenies TIgBls8zZ 
Thanasimus (Coleoptera: Cleridae) 
dubius' (Fabricius) a ac904s we niiiits » os See aa oes sie tins Dp ale se See en eee 402, 404 
undatulus Say vic0 is sc foes 2 one Saels ba pt ON Mite eine clan eee arilean Rae 398-400, 403, 535 
Thelephora terrestris Ehrh.:Fr ([Class Basidiomycetes] Aphyllophorales) .............---+++0ese000: 460 
Thelohania, see also Nosema (Microsporida: Thelohaniidae) ................ 00sec eee 276, 284, 286, 287 
solenopsae Knell, Allen & Hazard. oc 0 oc e coo o)s ce oa 0 wn opm wetness asta oe ee 286, 287 


Therioaphis (Homoptera: Aphididae) 
maculata (Buckton), see spotted alfalfa aphid 
trifolii (Monell), see yellow clover aphid 
Thielaviopsis basicola (Ber. & Broome) Ferraris [Class Hyphomycetes], see black root rot of bean 


thistle(S) is. cits olacdvccmcecte\s #97 slaw a ys wee Spee eee ee ey ss «nee ee 76, 78, 79, 82-84, 89 
Canada, see Canada thistle 
carduine (Asterales: Asteraceae, subfamily Carduinac)).: ... 2a. 22 Gers cance ee a on 
Carduus (see also Italian, musk, plumeless, and slenderflower thistles) ..................... 83, 88, 89 


Italian, see Italian thistle 

milk, see milk thistle 

musk, see musk thistle 

plumeless, see plumeless thistle 

Russian, see Russian thistle 

slenderflower, see slenderflower thistle 
Thomisidae/thomisid (Araneae), see crab spiders 


three-toed woodpecker; Picoides iridactylus 127. an. ane > oe ee ee eae ae ee 396, 400, 536 
thrips, Thysanopteta 7 . 3. =< Wese ss cm fee ae on ein eas wre tes > al th canes cat ete ee 331 
Thyridopteryx ephemeraeformis (Haworth) (Lepidoptera: Psychidae), see bagworm 
ticks ({Subclass Acari] Parasitiformes: Ixodidae) (see also spiroplasmas) ....................20005 305, 306 
toadflax, Dalmatian, see Dalmatian toadflax 
tobacco, Nicotiana tabacum”, 02>. .- e aeee n ere  e 14, 31, 32, 96, 97, 318 
tobacco 
budworm, Heliothis virescens (see also cytoplasmic polyhedrosis 
Virus [CPV ]}iere tice ace ee ee 30, 32, 62, 66, 70, 71, 279, 280, 288, 289, 292, 308, 310, 319 
flea beetle, Rpirix hirtipennis rr. no be ea oak Pe Od Sales SO a ae nie ae an ea ee ee 67 
hornworm, Manducd sexta tic. fc cei a eee ee ae ae ee 29,52, 11, 402 
leaf‘spot; Alfernaria alternata To. ce a: es oe re PC IS OF vas ae ae ae ee 96, 97 
Mosaic VITUS SPS Le Ee ere ee aN es ek grat een ae ay cee ae data ee 14 
"QTEEH MOSAIC™ FNS eid de. seh kel sank Ng aa RROAD Oo CRN ei oes eee ee 14 
"yellow mOsalC 27 site MET. SE LL a ah ees SNe ha alahe One aw ren en ee 14 
moth Ephestia elutella= srr PPR Avs rs Mater eon ara Ne Pe pee 299 
tomato, Lycopersicon esculentulifme in ata ae an ee ae ee 30, 60, 94, 98, 125, 318 
tomato 
fruitworm, see corn earworm 
hornworm, Manduca quinquemaculata® Pere. oan lee oes ee eee ee ee 29 
Tomicus piniperda (L.) (Coleoptera: Scolytidae), see "common pine shoot beetle" 
Tortticidae/tortricid (Lepidoptera) nose a eee ee 110, 409, 411, 428, 439, 444 
Torulopsis magnoliae Lodder & Kreger-van Rij ([Class Ascomycotina] Endomycetales: Endomycetaceae . 274 
SPP ees SEM PNY DT Pace le ad dna atin ocr ae Sener ator arp A pated oe ene ce er 233 
Torymidae/torymid (lymenoptera) \.22. 25s. an ee ne ee eee 439 
Toumeyella pini (King) (Homoptera: Coccidae), see "striped pine scale" 
Townsend's lonp-eared: bat) Plecotus townsendil a2 4. mot, wae ee ee 451 
Toxoptera citricida (Kirkaldy) (Homoptera: Aphididae), see brown citrus aphid 
Toxorhynchites (Diptera: Culicidae)! sims 02s <a eG iee oe a ee ee ee 285 


Trametes versicolor (L.:Fr.) Pilat ({Class Basidiomycetes] Aphyllophorales), see white rot of wood 

Trapa natans L. (Myrtales: Trapaceae), see water-chestnut 

trembling ‘aspen; Populus‘tremuloides: sx gee eee ee ieee 428 
Tribulus terrestris L. (Sapindales: Zygophyllaceae), see puncturevine 


630 


ar vearling |olasstiyphomycetcs em a erator. See eels o nels POM es cea ee ee 93, 94, 118, 463, 464 


ETT OP EN WEN A oe a ohn cu a5 clei SEER oe CR Ree ER Re ne Ton ee a are en 93 
lignorum Tode, = T. viride 
SJ Be aceca.rur. SoeGngiad, ogue: Coty eRe ER RA ee re ae ee ae ee | 118 
Soe EN RA 21 2 FN Ge AIS Glin So, 559 bes Gwe’ n a 4 Dao 93, 105, 107, 117, 118, 456, 464, 465 
Pits et eS A ae er Ee wnPak iin educa bP de 6 ge ae sae Swe Os we Pees vaded 93, 118, 463 
Trichogramma (Hymenoptera: Trichogrammatidae) ................. 10, 25, 26, 29-31, 51, 62, 65, 66, 304 
peuvede Navataia ce Naval katth emir seein ywaeny 6 Seg hs ptidia add Danica ahs hat ek witeouid 65 
ILS 1 CIht eee eter in tee ne ey oho gos ale ovis poe c’a 2 Okendne aa nae adwladales 139 
eT RO LUIINAGISUNIAE A ra an a Ae oe se aso os BALTES Sriadighenskd. sieneaw 124, 139 
PULINCSCEFS) WIESE OOC IE Br tonne ere se cs 2s oa W pal Ae canter ap arscad ada staat so 30-32, 65 
PAHO ING ac) DLAC Clann ree tee te Sicko us ahs oe Sas FS oa fe HSER RRS a RAS 30, 115, 446 
PETE Ce CET le me La Vs Seer REN te Oh hes sic tS scans one 5 4a\c cfioraeninaetane ote Meld tag OA 139,291 
STIS EL AIO OCU een Rn ee ee One Pe oy, Se eve oe eM ene vied Wo 124, 139 
DECTIOMU RACY mare Set Pare ware a itctars tinea t, Paes A chaag Yo! aww st he ben entew » esis 63, 65 
SCT LEPC ETE CL KALLS | ON PAE he Oe RM anny Oe hiatal na cas dial (dic ok Sales Bk Dee Pele wha a o Beye @aelaady 30 
1 8p Se costae pec ONS Okcap A009 61 0.34, OAC, RAR RIA ee ee 65, 66, 446 
irichomaiusanops ( Walker) (Hymenoptera: Pteromalidae) 2. antennae i iccwle ts fos err w lente ae cae oe 138 
Trichoplusia ni (Hiibner) (Lepidoptera: Noctuidae), see cabbage looper 
Trichouropoda australis Hirschmann ({Subclass Acari] Parasitiformes, Uropodidae) .................. 406 
Triticum spp. (Cyperales: Poaceae), see wheat 
Trogoderma (Coleoptera: Dermestidae) 
glabram (Herbst), see "glabrous cabinet beetle" 
granarium Everts, see khapra beetle 
CPB} Sweatt pheyiche ty oie apteyep Ry RW eo re ga Ceo a CRe ea te a eo a a ne re B27, 325 
Memes Ae «COCO DtCEA) are, he he ae Bio ees coe a eco cia Wis ae fue ss PE MA Ae eae 4 ators 335 
POD ICANSOGR AD OIC HNO! ATHIMN ICT IIN? ites fates vk. 78s aie BOs BVA fa, sitlow on el 9 slate Giga Wiatelatelc. 4,45 147, 148 
true firs, see fir(s) 
Tsuga (Pinales: Pinaceae) 
heterophylla (Raf.) Sarg., see western hemlock 
spp., see hemlock(s) 
Tuberculina [Class Hyphomycetes] 
TAXING ROSITHE ee AP ee. ee arene as eens Ce eee ee Se tle PIM WgulewlGaes ix eeealee sy 456 
ST en ee a oh tr a i er oS eis Siete Mentors: eae Eaheoenaitr game . wc ba ews 456 
furpellanians (| Phylum Piatyneiminthes, Class Turbellaria]) ©: 2.0... sete sewn. Ges eee eet 40 
Turdus migratorius Linnaeus ([Class Aves] Passeriformes: Muscicapidae) .....................0000. 536 
CHIP POG sLIPAPNIS CrySiMl yaad ee es es ee ee By eins also ois PP eee ITU ajo aia cites LEE 31 
twostriped grasshopper, Melanoplus bivittatus (see also crystalline array virus) ................... 360,312 
Aegraintaen | ClaSStA VES | PasSerilOrMes ) cis sa) 04 heen aids 2 bas soso oh daca rte TED . Hrghaegla’s 536 
Tyria jacobaeae (Linnaeus) (Lepidoptera: Arctiidae), see cinnabar moth 
U 
Ulex europaeus L. (Fabales: Fabaceae), see gorse 
Ulmus (Urticales: Ulmaceae) 
americana L., see American elm 
pumila L., see Siberian elm 
Unaspis euonymi (Comstock) (Homoptera: Diaspididae), see euonymus scale 
INP OnIV Ces KeGmidles ar UCCILNAC CAC) qa tarter | <tanitetcbs dine er aisle ni vinebccani'+ sis. ee May eae LEE 89 
appendiculatus (Pers.) Unger, see bean rust 
PTET CAS (OCTANE ORR os eet a Sos O's 4 oS sie, Kien on, 0 a s,s eyed Potaael arppend wel ot » 87 
RC TACN OVP LCT SIV CIM ene re ae fn ie dd Sas a's sp als aren elds Phe + ae a acco immbddwed & daerue 141 
SSIS nn ere Fem eco e edie clin mio him ce line apoE ote sumlanmemtlel Ls auia a 88 
REISE CULOC Lae I) II nos So beh ork oe «co > 9) Guage ptiag Gs spe Skee Ok ye, orga ers 141 
Urophora (Diptera: Tephritidae) 
WHO AEOU NETS OTS ON pele uso 8 fag Oe RO or Ce eo ee 85, 140 
Gungriasciata (NICISeN) ae aie ay «2-0 ee pees alata leg ates +E eed erate a 86, 140 
OSTEO AICO oom 2 ae OS EOLA? > COTO eI OE Cee eee eee 84 


V 
Vaccinium spp. (Ericales: Ericaceae), see blueberry, cranberry 
Vairimorpha (Microsporida: Burenellidae) 


heterosporum (Kellen &'Lindegren) 2.2: 2-4. .22sess205. ses ee eae dee ee eee 288 
invictaé Jouvenaz & Ellis= oc e So: 5 eee PASSE: RSs REA eRe Oe ee eee 286, 287 
Sp./Spp: ESC ePes 0S Gg Tae Coe Pe RP eee Ss a as ea hee hs ere cee ee 112, 288, 313 
"varnish-bush," see "tarbush" 
Varroa jacobsoni Oudemans ({Subclass Acari] Parasitiformes: Varroidae) ...................-.. 298, 324 
vedalia beetle; Rodolia cardinalis (0. oc. os hee ee oe ek whee eee ta at Oh Lek ERE Ee Sy ee 3,6 
vegetable weevil, ‘Listroderes difficilis 72254 2.00 Sasa bee eee ne ee ee 17, 25 
velvetbean caterpillar, Anticarsia gemmatalis: 0.22 e as oe = oe es © Be ie ee 54, 57 
velvetléat; Abutilon theophrasti .2 72.45.55 Fok beh eRe eee en eR eRe ee ee 76, 81, 89 
vespid(s)/Vespidae (Hymenoptera) |... ..< 5.3 saee cGk eae bas sys oe he eine eee On ee ee ee 448 
vetch bruchid, Bruchus brachialis: cs s55% «0.54 s oa: oes oa he ERE AE ORE 5 17, 24 
Vermivora ruficapilla (Wilson) ([Class Aves] Passeriformes: Emberizidae), see Nashville warbler 
Verticillium Wilt, ce.c0/36 iat oes dA GARE ees Ee EK Ge wml oe ee 95 
of maples,,Verticillium albo-atrum, V. dahlidea..2..2 tp. tetany ee ee ee 118, 457 
of potato and eggplant, Verticilliunt dahliae ... eae ee ee ee ee ee 94 


Verticillium [Class Hyphomycetes] 
albo-atrum Reinke & Berthier, see Verticillium wilt of maples 
dahliae Kleb, see Verticillium wilt of potato and eggplant, and of maples 


lecanti (AxZimmerm:) Viegas 5225 5 acs. 2 amnesia a 1 ee 92,414 
viburnum, Viburnum spp. (Dipsacales:.\Caprifoliaceae) |... sess feos oe ee oe ee ae 128 
Virginia 

pine, Pinus virginiana ie +. wes ential fot. R ee are eke het Os ee 107, 457 

pine.sawllysVeodiprion pratti prattiin..%en canna sees ee cee oe ee Oe ee ee 104, 114 
VITUS(ES) Wer ceeheonnit coe meetin: 158, 159, 270-272, 276, 277, 279-286, 288-292, 294, 298-313, 317-319, 


327-329, 414, 419, 424-426, 429, 432, 433, 435-438, 451, 452, 456, 458 
asco-, see ascoviruses 
baculo-, see baculoviruses 
calici-like, see calici-like viruses 
crystalline array, see crystalline array virus 
cytoplasmic polyhedrosis (CPV), see cytoplasmic polyhedrosis virus 
extracellular, see extracellular viruses 
filamentous, see filamentous virus 
granulosis (GV), see granulosis virus 
HIV, see human immunodeficiency virus 
inherent occult, see inherent occult viruses 
iridescent, see irridescent viruses 
non-occluded (NOV), see non-occluded viruses 
nuclear polyhedrosis (NPV), see nuclear polyhedrosis virus 
occluded, see occluded virus 
picorna-, see picornavirus 
polyhedral, see polyhedral virus 
polyhedrosis, see polyhedrosis virus 
Pox, see pox virus 
RNA, see RNA viruses 
TRV, see RNA viruses 


virus-like particles’ (75 SoC o's See aes aah 6 Ga es eee ee ee ee 281, 300, 456 
in Mexican bean beetle 247hufreo SE ROR RR oe ee eee eee 300 

Viscaceae (Santalales)} 2.5) os oa ay Pe ere a aS ae Oe ee eee 465 

Vitis spp. (Rhamnales: Vitaceae), see grape 

Voria ruralis (Fallen) (Diptera? Tachinidae) <223)e0 000204500 020000 Fede alae ee 30, 271 

Ww 

Wallrothriella arceuthobii (PK.) Sacc. = Caliciopsis arceuthobii 

walnut, Juglans sppoo eer ds 6 SS Re es 5 pa oe eee 279, 415, 462 


632 


warblers, ({Class Aves] Passeriformes: Emberizidae) (see also Nashville warbler) .................04. 447 
ETE OUEEC ICAL BN PIOCOPILS 1 CIVID ES acs), 5 12s. susicy) in HARUM Bio PARE Rls RI MIRIN B g wees a. she 311,63 
Pest ee yINeLODECES) 77d 5 nee AEs eee ec ek sa). MMe a fe 55, 63, 64, 69, 289, 304, 305 
eumenine, see eumenine 
vespid, see vespid(s) 
"water caltrop," see water-chestnut 


RePEc OuIIV pm OCIe Tl CVIN er ar ene eee Ly, hk Gh bore ¢ Kk see eke Ga ee Va 4 oe ARE oes 17 
ANaCENYVAOINC. LACHMOFIIG CPOSSIDES.. .cuwion nae as ar eee os 2 RRR, 38, 39, 77-81, 84, 86, 87, 161 
WALCELeLCUCE--F Sta SIVGIIO(GS.. » WANE. WNC A Vid ce BAT oat ah SR Sk hee es 77, 79, 80, 84, 86, 87 
watermilfoil, see Eurasian watermilfoil 
Rus ennnlnrOSes Ltd OIG. SUD aa meee ee cn Ace Mace albeeGit ya uniray 4 deca GA's a RR ew moels V4] 
MeuiaiG an ITUlt fly. -AnGsWeDNa ODNGUOR mame <EY Kee oe i Aue Oe 2 LEW ale BS es Se we 16 
western 
DIACKRGAGed DUC WORM CLEMIS C1 OUCIMNG tm ning Sali nks> 5 944 vrais dace ss hd od oA 101 
Romi roorworn, .iaprotica sirolera Virgierd 2... Oaounpihet Gea Week BoRlaNos Fhe 68, 317 
ESOTERIC KO SU OTC LOR OFT) 001 nie Meme a Sed SS ios net y avis wo aha ects Sine owas ow SROR A Wale oO 438 
HeNLO KAOODEL LG MUGING IS CEl CONIA PUCUDIOSCE temic GG ed we hn n nek d whe vai ae Gyn whe nto 116, 438 
Mat IY POE CIO CHICN S ONE cane ark ie Ret bok ice ate anaresos caine 4 RGU oh las on eww 441, 449 
Pa GORE AAO) OF CI COLT mare mse Otte oe ie Le AEs oes d 5G 952k > ape ae owe we HEME 29 
PRCT ety ACHONIG, DUS ICL LT @ Mat fetes i 05 a intro, lye ave aoc. MRIS RTD ek ae 8S: 9161. 411 
Somlce Sucwort. CHOrsiGneurd OCCIGERIAIIS .,.c Wao, An cacats Wh ose do8le babes wee 8 101-105, 444-451 
Sraeont seat mir IICG OUSCUNID CSE mami eek cme a ui ew Leu Gc, s SEO RAN Se 449 
SONIC al UIIEC I OIICO) Geert tats weir tals ACs ip ioe Br viet S DRI SOS Sac oe «> SRR ED 397-400 
wheat, Triticum spp. (see also take-all disease of wheat, Septoria leaf blotch of wheat) .. 90, 91, 94-96, 98, 121 
WHO AER FeTHN Sa MEY ECC ONITLSNCIICII, Siem mer ACME Be yl) 5 Vi gece aD ageatats io Sea a A ee 2 [6,24525 
white 
ae LeODNOI VIG Od OM Udell ce meme We Apter sie: hea DER. BGA «ae MN ee See Os 128 
eG IS AICLIC OU meine tee Th ech Ah iy coy uk aryl ek Gaetan o Rew Shwe ea ged wh dw Re 462 
BOSE ODN d SD) Mane ee aN a> She ook 8 taken tne AS Wes Sas as sole EMAL a 413, 414 
Beaci sede Ss CHUGUOCOUSIIS DCMUCOND wing was sie vied oad 2G ARs a ee OO me aed ons Pe TAL6 
DCR EUS SITOUUS wae ee AEE Mee SIM a os Oy A ee Sk tes BS Wale 438, 442, 456 
ime IStetrUst, 7 OMNI TIOICOIG Bie <a cieratis @ 2\c cls o> © a, s aera ety. ss Same alae 106, 442 
rot of wood, Irpex lacteus, Phlebia brevispora, Trametes versicolor ........0.000 000000 118, 463-465 
SST. RTECS TIO T” Boy 8 Sap ROR rit EO ae on OO CE Sone ee ee Weck end ere IE 450 
whitebrush, see Texas whitebrush 
Price SALCVIOCICaG. 1... vane eee irae Ste ERS. ats AG SN, Seisles ME SLE. 62 
pyoltemarked fleahopper, SPANGIONICUS GIDOLASCIAIUS 6.0: riceoireaep cin eiey beiine ove Asus wae sled seu hs 29 
Real ee eee siSD a mee re Nat oan ee nee ONE. hg ohana Ye a'e amuhg piss Ma bib kos ae kore 112, 415 
"arroyo," see arroyo willow 
PETIT EZS: UL. a 5 ., qeadbedeetbis tg Rec oar Sa tun ater eal OUP oP ea erro en en 427 


wilt(s), see Fusarium wilt, oak wilt, Verticillim wilt, "wilt disease" of gypsy moth, and also vascular 
wilt(s) in subject index 


"wilt disease" of gypsy moth, see also nuclear polyhedrosis virus of gypsy moth ..................... 424 
Winthemia manducae Sabrosky & DeLoach (Diptera: Tachinidae) ........... 0.0... 0c cece eee ene 29 
ete CUETO TS Oka! tee ECA eM wn ea Rs Oh ie eran suta aes ocean vi ote Gaede + < aan Vidae dua p gua ¥ ole 67 
site ane OMEN ee N TANI Geman iar  eree ANS acacia ar REE Naik a maie ed opie * oh ages +e oy IR 125 
Puetpaciic mie etlsiales: WOlDACHISE) Sein ne eg ovr sae Gea hi > ae ee hn Soc oe eye ew Ae se ace dine BO 276 
it a Cle ey Ch ea) Ne a a a ee ee atl Jus ie pana a eagle aa be ee 413 
mooupecwer(s) ([Class Aves] Piciformes; Picidae) cos. 400s es cb wrsasrecseens 108, 396, 397, 399, 413 


downy, see downy woodpecker 
hairy, see hairy woodpecker 
pileated, see pileated woodpecker 
three-toed, see three-toed woodpecker 
MIN EAND eran IC. eT IOSOMG4OWISC UI gins aimcypiegia.ey. oss SWE Sa aos eA naw as ee aw eee neds re aa 


633 


X 
Xanthium spp. (Asterales: Asteraceae), see cockleburs 
Xanthogalleruca luteola (Miiller) (Coleoptera: Chrysomelidae), see elm leaf beetle 
Xanthomonas ({Class Bacteria, Gram-negative aerobic rods & cocci] Pseudomonadaceae) 
campestris (Pammel 1895) Dowson 1939 
DVS. CHIT 15 ie aGin Bow foe nde ee ale Bees er Dale ws 8 oa layaee eos oe a nen ae a 97 
DVS» DUNE Rcidheciidte dc 9) 5 oie ecw eis oder aenye Siaid apes plaids @ Ale ale aera phe ots AME RmE eR ene 97 
citri (Hasse) Dowson, see citrus canker 
Xenopsylla cheopis Rothschild (Siphonaptera: Pulicidae), see oriental rat flea 


Xenorhabdus nematophilus (Poinar & Thomas 1965) ([Class Bacteria] Enterobacteriaceae)............. 452 
Xestia c-nigrum Linnaeus (Lepidoptera: Noctuidae), see "spotted cutworm" 
Xylocopa californica arizonensis Cresson (Hymenoptera: Anthophoridae) ............... 0.00. e eee 21S 
Xylocoris flavipes (Reuter) (Heteroptera: Anthocoridae), see warehouse pirate bug 
AYlophagidae (Diptera): .aieaytiuss anh ads «xe cee oe als ow © Son's CURR ENNR Cocle ncaa ct ee Ete gninS =n aneatee na 335 
Aylophagus.abdominalis Loew (Diptera; Xylophagidae):.. . sa¢s.e a. ose ee 535 
Y 
yeasts (Ascomycotina, Endomiycetaceac) i. 2.0...) ai crc o.s oe arc oe Giese ac Oe ee re 273, 274 
yellow 
clover aphid: Therioaphis:trifolit ks. .ccina cui cies 4 Puce, aby 0.4 ee PA 24 
pecan aphid, Monelliopsis pecanis, see aphids, pecan 
Starthistle, Gentaured SOISULIGLISi An... bles sce pie oss Foo. oe 1 eee 76, 78, 83, 84, 89, 162 
"yellow mosaic," see tobacco mosaic virus 
yellowfever mosquito, Aedes aegypti sine. Ga. teieeialn ee a Me Sn GR eo er 285 
yellowstriped armyworm, Spodoptera ornithogalli (see also multiply-occluded nuclear polyhedrosis 
WATS, [ANP Val irc sis Sota cite Sader Gotace eden’ «aslo eta ee RE apaee lee) cee Cg cach ee eo 308, 310 
Yponomeuta mallinellus Zeller (Lepidoptera: Yponomeutidae), see "apple ermine moth" 
Z 
Zea mays L. (Cyperales: Poaceae), see corn 
zebra caterpillar, Melanchra picta (see also nuclear polyhedrosis virus [NPV]) .................0e000s 300 


Zelleria (Lepidoptera: Yponomeutidae) 
haimbachi Busck, see pine needle sheathminer 
spp., see "needleminers" 
Zoophthora ([Class Zygomycetes] Entomophthorales: Entomophthoraceae) 
phytonomi (Arthur) Humber, Ben-Ze'ev & Kenneth, see alfalfa weevil fungus 
radicans (Brefeld), Bathos sy cise susad oncutegs. stasis ees She eee ee, 314, 330 


634 


NAME INDEX 
Compiled by S. M. Braxton 


Names of many additional involved persons may be found in the references cited sections of the main text and 
appendices. 


A 

ete SM) a eee erty en te i ees ty er Ey ey ay ea Oa bul CENTER A ule ie ee 299, 300, 302, 303 
LN INEE TGEVR) 2 ag eg ne gon Aaa pg Sen ton Ao 8 Ag a 285, 286, 408 
Deer RCe ATE GeV ia ey one ee Pea Ry Seems Lon CV as! es aac ceo owe Fy Ghee ella BB wed ae aha Nee 461 
ete BO BD © eeldam one Oi es he poe: Siege ino ic See a Oar a a 453 
EXO SEGTE Cs TID EIW ALS) cas ete Pd 2 5 ica areas: A: Ach eC Ee Rte ai et ER a a 80 
PICEA COMIN 01 Imma cle ren a a re Deira demeeve ete Sno seth cl bee b's ea CMM uete bed aoe Beier t 23 
OC Pewee A arrester, he ae tame ere rane) cat cael dled oh on hae bison S.A. Glaldnw pets 37, 50, 74, 78, 80, 82, 263 
Cenc ai NV ME rr NE Snes Meare Ree by ile De opeienadciaaw cate wi ecresthe Sas RS ek ew eat weeds S 18, 24 
OE ard ee Senso So ipcteeae MERE Act elvis: fe? Sten s: wad g ade slaecie ale shale elder hiv da eee da Pod 299 
dnsabentitee 12 ely ie ca es Bec! eal dont Bak! A) gale elas, 7) AOA TO) Sra Sas AREY RUD RU => oe rr 1S 
PM TILS ise UO he op raudee a Oncaaokere fie ate: ces nck ent a a CPt pe er ray A a Ar re 284 
ERENCE: SIDS Sa NeB oe tack Sey ny eabo.ns byt Chie lac Saar Ea A Ay OR ARR cr Cn 291 
Pe Ce ee eee ee eee ee et noes oe cole, Rete aidGr wwe ek Rls ee wate wh CA Gea DS 2 
See aE) Pe coat ee ren eee ae yg has che cay hoes See cok a dle ane eel fini a aS SR wiele os 6 433 
NOISES Sis. os Gath cate: oe ong cha 9) Bly ARREST TNS a Ea PUES Pear ec 281 
FATES SITS oy Sw gio Sik, ok Sine GUISE RLGPA culo: a0 RP RaRe OR i er PR arava r 4] 
B 

(REM Gce UEBUL. J aly A Pwr Oh GM Ge shel traf, S/R RIO INR A ae ee oe 283 
TET WE Wl Conch pcareet ey OMB Ar grade ue aan h SrtA RSL EREtey Or gr Sr RA ee ra ee RR a 81 
(SEY SL LARS: of Rane ore (caeameanhe p< Sih Aide tare Maem Aneta) 2h, fy FAN 7 7 Sr 324 
ENE RUE, oe OR eRe Mas BIB Sei oa ana Org Sank rye oR Atta a cr aS a 8 
eS a eee ee Boe Nene le Tce pes ee WR. Ake cece uote Tae wa teks winapi Mak Ces eae 94 
eer a See me ree ee cate eee hc eat ae rts. Wale uh ole artes we lela Wa a veka on TH, 19°80 
HBR ESE. Go 9 2 no BEG CEE Rien OA CEC ple ars) vn ior a RUN rpc a hg Sed a no A 286 
EMERY Le re orc eae tIA 5 crite oe Mae eithet aie a gule'e aoe aL cee ees we ee 16 
aA el aT rs thre eect Laat eee -o ie Ran hte fs eh iaresvanols Sate aid co Swag S's ate Std ee SE ae 83 
SUES eal © Cm ES Pe ence eee ete ee eye ae eraty see dart eis ebony a 4% 9 kad oye ne 41] 
Paral Se, 5 PO ene ree es cg tet a) oe oy Ruiner is see alehctedantllelsye dso's gteré wie ha dda tune ee eo 452 
VERY. UIANS oo oo bi ethane Aire OMe Cy ee MIRO Ty GEL Br 0 Ge Supe ee 100 
G@eTCILAGIE . seecteh date on fig Spe Saenger are Sara ae 285, 295 
CGH CML. yh cael Rhona oni SRR 1 2. Ghee ain ai Lae Cc Arico aoe a a a 320,321 
ee ee ee nee Lee ME Rr ee Vahl s s bliieee cha Se kee} Sao we EMR BCMA oo 411 
ee ee ee ah Ns Pa EA Toys Ringe k ev ey ees Be peek bee nee 4 AeA? 
See a ee Ee oe tern nana e bias.s cuieyaeh wtih else ld his b@ As es BE BA Ge nee 88, 89 
Reiiet my at arene ee en Peet hia seit bce aits ean mrtg cl Maewlt 4h 4a'a Bred ee 6 Sa 406, 407, 432 
'SESTYSIG, cogs Ste ecb yeti g optec cutee oy eer SPE Sere Beg rae ign a a ara a 324 
Seri ak Me er ee ate ay eer sURN cline vida.) china cic oa ely hse oty pte #8 Ble ean 436, 445 
erste ey eee ee eee gor nets yy ares bt daa teed Shas ewan oe ea tile os 455 
chin ee ee ee Pea eet ome es oe eG ty eae Aa om Wek oo ON aba ed aie ee ae ee 17 
EERE ER 05 sou oe wie 25,8 Rane ey ES er ee 308, 309, 327, 415 
SAE TRTEL oo on lee shape gealealo tg ogee ce ae Un a 81 


635 


Boswell, ViRo co. . cos sce iS alasece ae aa Ww ru aw eB area tig ae ate abe, Sil al cieeine efoto ea nee ees 40 


Boudreaux, Hi. Bassin sastia a) shesitin begiaspuiizr tes, Gimmes Geaw be babrmeyas ov tev ve gi ahh ee tte, eats Sera ee tie esas ee 406 
Boyette; C.D...» «:esssad oS Reet baa ata oe Read aust Re ob ae aioe ces tee eee eon ar ee 89 
Bradley, Danas sveide ¢ Wes taSin\ Clnawatigs muapetouias ge prehe« Seber <fe aigh oak tows cae e a neg eae 415 
Bradley; WG. gthearesnu's ROE im tees BS ae 2 Se setae 3s ae cpap le aceueon st sy een 291 
Briaricd,, JA sie erected Sosa, 5h 5 we ae ba ipa hs VES NEL a Peat eke ges eer eae a 286, 287 
Browtt, RoC esreused ecb ks ieee Ses ie eat Wak Saas eb A Dales cha WINN eal ME IR eee ae 409 
Brubaker, Ri Wieei 3 Seaeteds aed airs Petia dene ae Wine ch BB cn we ee ree 29, 30 
Bruices WHA sed cecal Bt atte hal eae lt prt Secession hi ar dion tae sre cee ee yo 298 
Bruckart, {Wa sccrasyarcheccuns 4 Peervad St EE sltacek Rd ee es Be ren ae ee 88, 114 
Bruen: RB pecsine kr ctenicte cousn ad saae-eoclareniea lease ieee eames elt ees ce cae rea cli toi ert ee 426 
Bfumson, IM Ble tect nats csv hie tysdlitteed sd, Tatiyeitete 2 dete ele mea cat cs dae Reis eda TRIN. ecu h eye cc ene ee 24 
Bryati Cs rccerians BStrdane Ss Wheat cicwsae ee ches ih. valkyrie ao ens. eh ves ean ae) Oa kaae eee ag, a ee 459 
Bryant) Bie ce Py crsni ch. «ss eei-a. ols) a a wins os Se aelenee cialis neler ate es ear ere ee een 44-47, 263 
Buckingham, 5 Row Mel fads aioe nihidee Ais SMe dtecrmeturn Sea agi sei re wetncagle het Si gC oc Rae or 76, 79, 144 
Bi fiangs Pele eee ses -a.05e. dye Goals: aianas as ovale noe soba tana ete eee cnceale alana Ge eee RS. cane faleean ae oh re 454 
SLEW ORY. ah nee ere een ty enon ery een ein er er eR Eyal Glee: oo Se 263, 292, 293 
Barents (WPS ape ante 3B itestinntivr ss emaues apie estrecho Sosa da ele af a al AS by 2 GR UR PES | STS sare 285 
13)01 6:23 ol 04 Deen eee ar OY ee ree eee Neer WRrecte oa eens hin ean kA A ak oR een sc [22 
BBUINSIGe GC tity 6. OS Lie teh te Pateatars, Ua Pees dent Men 22a cit in ik eee 20, 296, 297 
Burrell sR We soo has cpne ed hates ewes RMS See ate. ag SEO Rhy Ps sir Bl sce gS CNG Ate alee A Re a 16 
C 

CACSar An Te pete gree se. hte canoes eels ec say etereaeek heat Sa chagel ade 4 kareena ee ah ona oe Cae 79, 89, 90 
CalderemesN W ses waters svar cc Srveatand Ldinlw is Steed ance ARs eee a atest Pecos oi cee) ee 298 
Cameroons [eWay Pais S5eco are 0 G5, oe she) ape hence oucccee eras oe ge MAIN AiR Ese Le a 34 
Campbell Re Ws. Qrcaclbas co alraie Senimndiusis Sf i oalaeiiins wane SAE “cout tain) ae lester eee ee cre 417, 446 
Cantelos We Ws sau cise ted creck, poral make Sitar So oes alee Resta yl Oeeeeteee <a eee tins urct Ra re cea ee 68 
Bantwelh GB ve oad sac hcee leg eee ake eae eee en ne ot nee 297, 299, 300 
Carlson: RiW)4c7-iepad e's Saperstein pager. Sock thc PUR AIR rune ocaes B5e 5 Ale tpee sd ahisten ae ee 55 
Carruthers: Robin vata eca aa Genes tek cade, Soybean Ota fs oC 145, 152 
Garson Bache liege: .eenchcte ter tad in iepagus oie aimee dug re eran ate Gels an RR ee oe 28, 29, 40 
Castellanos, Mike Wisssos mesg en Wee tore te coled emcee enn 1g estes cual ntti <2 aaah Ree are 461 
Cate, JaIR pert, les seid haces Motch Pe crc: « ste Mies VR e RI ashe © BVP Spee cvs ler a cue «Sant a 63, 144 
Centers: 0D. eX Syens ees aeeveewsat ete cade, <A oretas aaa ae clo tanith ic Daisy dee tac Sioa cu ie Site tele 80 
Ghambers.s W..E.? tapdvcc’s tate, mes, St ayaa Ae Ae Saas Sauer aged Raa cect tia Nec gil eee See er er 12 
Chante lett: Te Miagt pte) 9% cao 50.5 5.25.3. 3° +c dua Ae aide eka cate stoke ey 0 Ba von ola eee tk eee 81 
Chapman A Ci 52 ane ate oon gas y saci ae ere agen EAS oh eee Sac AP a AE Re ee 293-296 
Chawvitty RL ysis Se. ina cm Stee 0) Sn mete REE ERE Oe ale aes oe, rete eg 327 
Chidester, Mi Sse a5 4a Gi 3 ayetn 1 xsi Reto Cece Mel eRe ts phe) ere Gm 463 
CIUtWOOG DTH sega oo Gbd, whsan ng aiulooihon/e aya Wrest Un ReUeE URE NOMUUE Sark a-sialon 91 
(Christensen, CBee ot cea sSese eae © dias te, who ene aR Ret OY eR mS ns ee re RC a 269 
Christies J. Revs: sates Macguss dukes 00 «Sie iting, nage cones, ome ae te aoe Li, 12522 
Caverolo; Bolo. erst sins Sc oeany cs hear b olen lo Ol ante Cee ae GR ge NS ee 97 
Clancy, Di. Wasa och 16) sk co nditg nero gar ayau tO ORe ane Suen ine mee liye ce he fe eat ae 24 
CT Ark, FBS ox Mme eects dh Doe ceo aca! he nn AARP em eC eOR LAE hate at Od Ser a OG Ca 22 
CLAN a BB eg aie hc atte hes, Bo ot Gah Pah ck SR od ae 280, 281, 294, 295, 298, 303, 305, 306 
OIE <A Mae eC eee ee ee Ne enter kotor ee Se oe ete Me, 455 
Chausen, CP secs pegre!n piar esse db de he Re gia « Siler ate me Oca aa ee a 15, 50 
Clement, S20 cscs. 3, Fr bruins scsideas igo tiga: 2 ateteee Ae taeee eee REN A pert nee ae ne 78, 84 
Chimtonn, Waals. 3. ars :sjhs Ate Segiace obi fo, soni a pao ocean cr ea cree | 154, 155 
Cloud, Ru Ver dsie 4 siwsa ia areca dow aot ote > ved acs ac eeeiaite ort Ae re aera oe rr 293, 296 
CODD s INAS ocscoe ch eydese d's. eciigtyeitenet otha 0-5 okey aiaete epstn veCR ok ne ey PER eR a ee LOsb2 
COND Ore, Fare ein ice tenes a tocaien ian e ude gg 40h cok nie. = se mateo RAUR cee ce a eee 445 
Coles, LW cu oinals taba ctied aie sslss & 0 e dinette oto aetereteae: Oicnes cen es eect ge eS ee ee 24 
Colbiras, As ge sme Sous fects Soul nee 08 Gs, © coi cus. cee cid ec ee 324 
Comstock, J citric aveie aio c's son 00) sim tua te ee ane eh ras 6 


636 














ne a ee ee BY when E CR RAM itis 4 hve lacs lalla 8 RON a Klvck se ks we wo wd a oO bodles 428 


CASES, Us li oven Add het et 2 Ae eg ee ne oe a 41,94 
hae (ale 5 od dae dea s.6 S54 Se uae ee es ee er a ee ee reer ee fig) 
Sew arr ee ee ee PE ee wee PE Fe «5,15 sg hos eS Paes Rusa alowed We Decce gab Jove wd ate | ER eng 
eden Te ls Re eS OO EN i 5 HE Petes Ye tc rind ieest ae Rig ba Gn Yo lena ios too won oe. a ba lavelle e WAR Rows S0R263 
Sy a ae ea FeO Ew Re AM GNC ek: Cae Ree hogs 85 cali carauc Make Alpin Sassi Sete arma oe'enn rma oreo Rees 312 
CON LEWD aye 8 ee Eee gees BA OE AN ee 0 ce Ree tet ek ln ne ne Oe 23 
Ol ess a Peart ea ae ne wise Vs diel SNe cotin Foes jovand due caaecsds nies eae ube oe 445-447 
1 Cs) GOSS: oO EMP oe PR 8 ot hd ee rn 0 68 
COS one eA Ce eh oe fot oe ale ae hey a a rr: 453 
ROS yc 2 SEN, Oy I ee ee ye ees oe ht ee ne er oF 406 
OTC UR OBER Tee ee Be a Se OA, 04 Ae ee ro 121 
LEDS Fre ck be CM oe Ore I Weal i SP re Sg gh 5 Fah fabdrs Sash odes Silas Abele av'w, sub > dere dra. 'nnlbstowe eda ohh 316 
D 

Sta SEG Tai SON ae Sk eee ee oe ad a Geer ON 4 Oot ene nC eee a 433, 434 
AAA EATS ae CT lal Pee Tice WE EET Sv PalesWes ovo eile tin ols Sn Mi ME (bE huts al aynrte a raed d Ow RM 311 
LOM CLE ag Obhas, Cosine the Sonene anced © Acie Gen a Rca ae er er 40, 41 
CUBINDICE SEAT Se Daten na epee ath Pee oc ene en one ee ee eu} 
Bibl WaT 2 oe Sol Pavecs Rea a CnORS caches Cea aA EO ak eee. ) a 24, 56 
ee TCT aem  RE Pey Aoa  coee ee Pe  ea ss a tortie tle ere hE 9 WS, aie DR Caw Wa He EN 287 
ea eT ine RT ae Mi ait treo Ue APO Res esto tegen Aes ea Pictorial 0% lat a's Wht Blallnns we Sea! apr ys Gio aen sare oie ODE 455 
a ee Co eal PEW secrecy ARN IMC ey ect os 1) AIK os Sil ar le Bile Ge Ph ecb ceile ae’ MS peste wages eh eR 89 
Peer EERAACICD Ps AK IRL ae tee en Sth aly Gen, & Ac eat Al af Siw) wh bh gran e/w aloredd G ales wh wRSe 298 
LCN Gs EE 5 MP Nee R rete hs Le Ala ce Ae ne AS aIW Win Sa Seka d+ oR 9 brian hw eee 122424 Seal 
Tyumen GOS O® RS 2 ese apm ee at are ee a a eee > Oc B38, 500 (4a Tee leoe 
CE aC RE ea eae hel Oe VE TR ales L gtetl Shc us Se et Wi 7ehearn ee ee Shleri GNa Ge Bao Geiss iw ar-ay ni’ AO Weis a Ha 441, 450 
Beer ater CN ac Aa ere ee EGR hate rahe ler, nga aun Pala ant whe W Shanda Aras eral atte ale saree eM 417 
PIT ar Ta nD Ss RN eee ese Pr a WEL a Sy fe dis, Vasa wad HE A eR AMOS A's wn Whiwada mabboe le a4 450 
UPS MLE , ea a Qe A oo ee ee ees 412, 427 
et CE VL ae Ie ee ey I el Ba ath oS RAD Seda EGY oth BYES wes Bae Paes 301, 302, 304 
er ete eee ays oa NE wien eR a HAR MV OY RES Gee ea 100, 416, 424, 440, 441, 453 
re Ne Pee ee See RMN Ra RE AA ods nin tein bea BY ANH apd Bs 24, 37,47, 51, S449 
ERIC a ay hee Ey teas Nice aun alata ales BETES Wd Gore We eve heen ean Oe Zien 
OO Zane We Pere ere eens Ge es Ee ER ee es Kis SOROS we MR SAE WEG 104, 415, 416, 433, 438, 444 
TC SR UO eae he PP ue et ce ane EO Ee pty a fats SARE fale imi uw (ger eth BAR 428, 429 
eT eee) ee ee eet eee ar oP ee rs renee iid edn jor site foi Sih oa ae ga Noles Mak he AY Ree RRA 81 
Das emt eee 2 naa hee ene Rak, WES foes ee Len ei ee Sew ME he we Oe 2 34, 291, 320-322 
OTA NEG, 4 Sather en a eee ee ee ee eee ee 37 10278) 85 
See | ae ee eAras errah ee ee rR oe Biase A MAY MRSA EH Aa bs oa Des see PES 426 
RY ie ee nie inet ati Dini RE HG doe kaa IRIE BOAO ea ws 12, 20, 33, 289, 298, 299 
Lact eee) Men Cee es cht et matolad solr ers hewn cas Sha ee R ES we Phe Lage ved Cees 24,56, 38 
E 

ey ais rn nt ORT 2 i toate he GRO Re eka ee shah sia wle wa Won 8 Medea $1 
erie d) Se. hee dey eden ed GL en SOR Ge IGE Ore nn aa ene ae ae ee eo 422 
RCH a oy RE ee Se, aS Cheatin Gaby Goeasiteb Sia whole wh ee wa a Ode ee ee OR 97 
Pease aes oe nO eae ee vas tA tat Ss ph MR WM Sn Werte w es alee FO Gee ww ole See Ye 281 
Penge at Gee eee een Cera ion et as kk EA OLS LES RAGS OG OF Co CRA wees naam 88 
Aen oS ee I ee Si ack yp WR ied sei KW AS bw his unyy ew Vb ew whee ae be ag 45, 263 
Ce Mee A te ee eee AMR REG a Rh sys DORA TENAM ORE oe WRK eee ee a eb EAN 435 
F 

yeaperrreny Jk 8 Toa Ago ach enc aoe ea Se. ee i i 331 
Pes OS eee ee Pe eon ae re ORG MEO RG FER REGEN A esha G nt bbe oe ASA hab wwe SO ESO 68 
Pugh RAM ag 5 yo) Were Lenk tc og) Aa oe a 299, 300 
CRE PRE AE ERTERRNIER GABA MER CREME GSH RIL RESO HELE RN ER DSS See ha oe 415, 416, 454 


637 


FEUER Y Hel ic dos atic hed digg kb etl aed He Pe od alte aus bt nocste do fest Lcahobne 2 2 et face ea 415,416 


Federici BiAl i Se wee odious Cdlw vuhon MRO SOR Ml aye Sore ene 6 aheansee Bk eee ha ee 285 
Féldlaufer: M.FY cc ada wise 6 atk 5 oid Settee as Wie an pete oer de ere Reger go are AS Nh To a ee 303 
FLOWS) Hs ed oid sos SR PBS Aidan aheer evade ela tert a tee e foce Ae EN Ege wo Salto ep ee Re ee 22 
Ferkovich, SiMe sitio ho De aid ok Goa ueee eet atte er cone. Sue enero yell elPeves ert Goer ar eee a 303 
PICKS CH cb bew css alphas ele inane ob ater au one tee tase asters egeaatl oes Gori opte ae 22 
ETtCHSA Pte ses ctig sid ee thw Pee ea dhe ade Shale, at emt vot ie ey oloyone an sare tatie {han oleae ae edteg eee 6 
Fleming’ W Be c8 hacen ais baw a ade rss gp eter es a pn owee ee et nlite teeTe)ek  iea ee oi5 
ae 5 0.) on errr ree eerie n torn er. rain cctriir em ems PEN Or emia ee A ihe % oo. 2 272 
| ta) co € eee ari eee Meret. ee Mr PU nee a RN REA ann io H crake Crk IS Lack © 435 
Sieg Fo) = Ol Chea eee meee ee RR i omer 11, ft fee Pree Mie Penk Serer ANC eer ee hs OF A 131,142 
POrnaSaty Lae Fs. chsctalcdnd aisc.cawal Soaked eek yes isles AI eam awe) Vag gO ele ssa lathesetas tae tngeacs men chee cit-t ain 84 
| ei6> 2h | = Ree ae rc ar un Sa eect te rn ane a hora ene PAREN RS resem nin ACh sake petra Ap co 12 
Prank? JHE coop fa Peer a tee a ce See SU ES tse ed oi Aimee oe GaSe Re ere oy a 144 
Preys RG) nce tm oy eal dvi a tbs SPE, «nD eter es Gla To ie ganda s erica A pastes O09 ee ee ee 144 
| diy (ol teh CY tg eae Pe NCR an PRE CORMIER co Vic PRR MOMMA a TM a AIOE os ulin on 37, 81 
FUeStere RE W ca gee leN ears been eat see at Mica Ratec cde ames teh os tien Ae Sok aetna ie ek nae 56 
[itll (at id iy eee Ce ee a me arent Vite Se MRT St ent od wee eeu TS Rint neta Se eg 285, 294-296 
Beart SS 5 RD apse sabes Sigh Rs stn oes cath i See Pire eh Bead onteatat es foes ce oR attes sureties eke nn a 435 
G 

Gardiner; VR feces Goss fates, Soe bacon sir op ots om spre oe hy ecg tal oe + zo PL ts SP Rn 16, 18 
CE Pkg Ko | dhe ol B Pac ta SN ae ane ee ee ROG eae ian eee eA ae ee GMa apis wo eo 3 93 
Gaskallas Rit catx ess eis Rants ieee ich te eam el Seg taps opcnobaauccco) oan a reat eee 144 
Ghiertt PUSH e a Steg So a Bids ae ela ee ioe, Bie eens ern ele Re ee 438 
Guar 1 ae Sari Sis ec alk lg aise onle ve teas ea ee ei ce se tenet corr its ch ile Rare eer ea 273-275 
GINGTICR YR Be ys Cae a soe Bes Sh RI he ei eels a aes te wore ae ere ae 321 
PETERS ee aa Ra ee eee are ee ee ie oon) aerate re ee ama es en - 12 
CICS oMh a8 shed | tena es ened Ae UR ee Sere eit haut tnr sand et ene LM OL KE dhe A Oe 5 293, 296 
CHOSE OLA TW ee. ae See es los tele ta ol tes et ae ee eect ee 132, 133, 1422043 
CHRO VETO PRR Oe oh ch alt Seis, Gah ie a a a ec pee ences dee meet, woe shi a, een occa eet 6 
Grainy BRAG ake are 4 GN Sears eRe eae gs Ree kane tee toe eee acces aeaeealctr opine eee 416, 420 
COO FRIMicgS ed G AE ory costa 2G SCs Oe ee eee ee, Re ae er Nr ogc ee ee ee 33, 40 
Goodwint Ras 4G See eS elas eo ee te eee et te he crest org eee ee 301-303 
GOTO IM Tee ee NE oe a eR re oes Suara em? a ern er 293 
GRACE IS Fig AB Shs A Oa eet ke ae eee, ee ote nee ance te ar ae a 301 
Csreenstone? M Hid 5 im oS Ra ela tele oleate ts tater ee aoe ey out aa: le cies lee ee cee 310 
Cor SSI EL Rte Ay foes ep it ek ne a toe ee ee 0 te ra 62 
ASTUBCER Fs Gh em es eee ees aaNet he aes nee te cee nae eee 330 
Chr itty eh Qa a ge eee ae ae re ae enka gg aa a ARIE A herr des Awe AE Se Ag iS ig 6 5 302 
GUTOR DD ee oh te EAS ie eles ay eS ee eae ee oa ea tae tear eae Re aa ree on 302 
H 

Habeck: Dees 6 (ce) ae bc 4 lal Bc ies ee eae ae me rte ie) RO 79 
Hackett, Ko; sree, sic wes cracks ak Pre ae tee en ieee ee ee es ee 145, 303, 305 
Hacskaylo,. Eis x Pets bie own’ G mS Si Sree ak 8 Ra ee ae re caer hoe eee ere ea ae 459 
Haetisslers G. Je @ cs 4-8 Siesta A Ee Ne Se ces eee ore ee Oe ee er 8 
Hains BUD osnastd ole drive Qos tee © thar Sic ore Seer Retreat Peele ene: cee ttn okt ak ee 423 
Haissig, Ky 2 esa Se 6865 Sahel ee cee ere pee ey cat eee ae reer eee a 450 
Hal SDD reg ac) sted Bs Sw BE A ae BIS et id ST ee Rd a et a 285 
Hambleton JeD, asco o's hess ein eeu egy A Cpe et isha RS oe Eee eee ee 18, 20, 296 
Hasrmigs Ja, as. 53-o is % ekg RE ee AS a a ree me cs re ee ene 288, 304 
Hanson ;"AsA. «225s 3 4 es 09 de a ete ee 49 
Hardeés:DsDs secs pi 8 aaah Sm a eet eee ue ce Oe ee eRe ay | 
Fharkey Mer iia tse cpt eas ots ol bn SHES eRe eae ENS he Cie ee se meee 415 
Hartleye Gy tie a teg 2:5. preovie oreosmuclute, olla Boal al 6 em aR vie PL ee ge 13 
Harvey An fovea 4 ihd a dda wale 8 Bie Gia wae a dae Biden eee te Oe ena Gee ote les caer ae ee ae ne 462 


638 


ee ae) ee ee Ue gy cay Sulake A ww Sais & wi mG Nias Gedl ab Aaraa@ nda 37, 78 
ee Lee Ce Cl a ne aOR © ee reds 8 ete EP A, oa9, Gude & Wibdlspie stale tele n'a # wile TS wwe a ov « Pabhaty 100 
OMG, Ueinte 2s ayes 8s ek Cae ple Gry ns Brice Se en oe a Oc oS a 12520 
IMIEYBIT et, TEM cet Sule Sieh OPES Oy REY Or cag RGM SSC ASE GEPICTLEL e OR 283-286, 295 
Pee PUTA TAT Orter R ric APROME Be aac BEER Ak ca ild tc ube Je Waive. & ip lie ard velba wile on wah hates bheOA vs 54 
1a OAV! OMI On ae os JOD pre gig Se a en) te 34, 263, 299 
CLT AVY tLe oe peerte oe BaF Oe re een 7k tr ete RE PUN RU Faye ticles du laa vel alls slatibiie Sa lleiattevieridls wee uerata 1330 1326142 
FEES Oe es en Meer 7 ee te Ee on Bers ae ete Sao io va aa Be naw wig a cal a “oa bea ate 285 
LTRs, MES 9 ila dS are One ier SA a Roa aoe So any eS ent As Bi Pe ce ce ee ree 311-313 
PETER ME ES Vor) Fe pee he ea ie eee OO ty BD ar AD ey aS LNT Fs Ay vale salloie ha Wighte -elce inalie AObHvobin pu yh gh al eee pre 298 
Wiel AMO, SOO en ely a GA RU kh 20S, 2 en Oe ee oo rer ae ee 293 
PUT SL Se Wy okt 6 ESOS ASA dat 8 ches a's 4), oa eee en Cee ee re 83 
De NAS PRRODY 0 Pas a Tw gt a aM Are En Sg eg alg CAR balians aPehtvis a a aisle tw avaidte Beece ORS 29 
TWO OE LDIF saucs eee Pree maa: hy ind A ake BR ee ne ee en reat 328 
MACs a 6 oEyatee hn bt a & Abt ak © Bey AN 6, Oe, Pk Gn 2 a re er? 462 
PCrE RT aTISD oe 1 ee ae ee wy GN A Wey Aer he Tee A Wer 5 BA eictaeuds peak sue aligh abn tact d-sietal debve’ weced OE 23 
RS err ELSON CIE ELLE INGLY Romeo init Goat Sete MeN an nem Ree gE RCGR RM th ot chs L nua ly ianilood Urns asta ah edhe abvhidbste: ee sha alae Shoe 415 
EIS MONC Ep URL Ser oe heed & SURE a Bin noe ty Aue om it Be Qin. ons Raia he nee ae ne 18, 21524537 
FSG SWE a Aas BEB ose ils Rone ig Bi ter ys ok Pe fon ee, 20297 
IRM Tie yaks els Wc ee A pone te Ga eld be | A ea en eee 147 
JPRS CT IBY bags ticity os aS E IEWE LAB PEED OAT Ep BA, UG Faun aed cea eee ae ae ee eee a 308 
PEELS RALLY Lo Vy Set poi te ee ea are A eB gd oh eg eatin ON alist ap Ahem ay sete mee vedio ane aahetees 9 NN 448 
EC ESUEE ED oem ee eta tana oer feet SRI Gees eon, HOS HATS a4 fas abs Set aEe Aaa aR Ce a ew Od 132, 142 
POL CArc as O) Grr oe he Re EE ee ae RPE Bah aed hat ath hchare gae od wee ane’ 6, 8,9 
Vetere Ut sin eee ee ee RN Aes oh hcl ME De, bade wien didn dens waar et weeds 95 
Vet ee ey Nee aes ernest ise PR OY Ae Aart SAS, ARMAS ino hai hdd oat ews acad wathee OM S27 
Bev LEICA nena § uchleg en eA hg eC OY i hoo ae eget ra Sorts (a dee a Re ah ih de Row a dave steve Moe 281 
EAC aN te eee era rye ee A Ae Aa tA oo SO Vila daa dk dues dead eow added 4 135 
ayy ees Ce ee fe eer em RT SARA culo aaa a ds eee mA ciala ENO OA alae ALAM NOR Is 
PD ait ee aL s ae ne en ee ee) A eee ee Oe nr eS Ra es Sea np ee kaa Sole ey Fake OwS 426 
CLC TaN et et ie eee Nae Ms RSet AO hs 5 Suited wee den ahead Oran eee 91,92 
PDE ECRAome eee Se ee Oe SRA Seip ners SRS Rak ea MRS Ae ao eha es Ae 70, 159, 314 
PRT AT es Ey eee ea ote ee ee Ak CaO A DBAS eR US MEN BAGO A LAMAN de Fe ole QU 304 
Per a a tae ree een ey I AW Tih a ois 4 ANE oo ab BNie Ded Oe AD Ow Sea he 279 
Lorn ne ome a em oem eho NOES SNR CG Say hs ce Salas 6 Pee ae RSLS RM ES CRS Toe AERO 142 
RUC HINS eS a ae A ee a ey ths PES Nt An eRe ENS aa E Na he noe do Pee 437 
I 

Rot OR CONV EEIMME PAN e Na aro eas teen ae ah thins Ree hs Gar kee 25,32, 263,307, 309; 310;3:17-319 
ae ee een OO ere ees iy aUN os Aas Sn Abad oS GALSIAS He ayw h Ohb S.98 A wa eed 299 
PAT ee te Fn el At dae, Fe TA Game AAS See. tawida Yee ove ERR 87 
J 

Leta EEE I Lele 0 oso huShcy Sate ORE GRRE ARE BRC ie PORE RELES COEI TRE CLAD Sante ar gr ar ae 68 
PAC SOIN a Gt en ei are ite) ere eh Oe rattle floss ei ade sth ate 9\s b+ ela ves a deh OG 47 
DAL SiC WiC 2a nn Ome ous ee te ee ee irsaii nit ae tnd din Bae Wi ears AM Aww 6 sees 98 
Pennies eee eee eee ts Pn aos memen at ivewa ye PRR tee ET ¥e rudy a 411, 412, 439, 445-448 
NOR SCt tL) een eran nee a Me nny Aan eG EM eR Ae aha ay fas Sad + wale EwR 292, 293 
SST Sem) Si tate ee ene Ce PAU ete oly nih aise (oie 5, ound iad wale @ ai bowbrw Wes Ape 'd ec eles BR 18, 24 
2PORRCI DBRS Bao 3 coc A Al A eg ten oe 285-287 
Dore Tisai meer etre ey Are er eye ieiew ty ahh We hiv eins 454 bo es MENA EO ha Ws oa RS 462 
K 

COWES IETS, 55 0) oie olen Oats Bibi Par Oly ect 8 et Sea) OCR a Ipnet are Ee DOE Sc Gora Shc ar eae ar mee OE 287 
(PETES, SERA go teedo. agile es eos APES coi gp 276, 277, 294 
PMY Oi oh ou a ohn toemaQh CORNY Glee SGU He ir ion a Oke are ee ee eee 285 
CROC IED ae ee eth eee cL eae Stns wails Wa VRE GA she Koay DEN ew sal Oewh 269 


639 


Kennedys Bula sc sec aya avacsea hye sees iy et aim se erie Heed bby gan Nae ee ee oe 100, 401 


RC PEVS BER otisoid ag bei eee ota es wi aan A cogent IS encore 0 ce ea 91 
Behan eK 5 Bet ee hess a en tes Rone Siva Sa fo dpslgbareae fo dihceln ee oiaeo lk edal tigettk ne ese ec ee Als 
KinGaid sD Re eave: i id ene Gi jpoeepcs nina ssc aati bie te iecstdetoe au naive ie ce hoe Abgieseiedtens goth kee eee ara ge 47 
Kimesolvers Geli. ok. cbs. 0d yo ho apt anere eee Bees nin teseoyen ob A sein gd ae eet tO arene ne ee 88 
BeTSHa, DAB RA, eich ov ames vpn igs hare ON RT le eee ete cc Re 324-326 
Kbass@rad Wh bars. 2. Kine, duane wn bisdim sesso: stesso pet oedemeals lets ur Poe ge Ses Scat ae eine pete suena eareareeck Ree cone ae ere 2 47 
UAL ANG 0 © en DoE RMT EN IME Regis ome ot. PKC AW erin ela cepre TE & EM aS aR lant ch hong hel oe 68, 315, 316%334 
FLSA WEL. 5 sscieh  soind ese, colle on uv gu tess v sheueis Oke eee seat ce ade cep a ge a 450 
Sit Me De ne eer, ee ex rte eee arty OM eM Oc ye ro vod Ss 285 
Kindo ling, Bic oi sotteracs eae suede aeons aca ace oe ics Rs edo a 142 
Koairp linn RF sscac aan vassouatas nee cgy Soehgbeeag atta lace wha ee pegged aon ae ky eee ohm at eae eae 23,331 om 
PORE Dy Act a tac sarees ogee cies peda Pacsafe oh wea siea Sea va added gaint cougar ee 297, 298 
Ai iicte 60) Eee on eee ee AT Mn RAOULT ATR MN CP Ol NS Da oN nh BO SEM ny Ble 50, 54, 55, 76 
1400) (a; OE ee ee ER ee ee Re aT MRM ET AT SR MER ek pS iow 6 
RiQllees GN. sc icseech keh, ceca yale cates PORE Dac cersacaiek hdl ale yin ge ae 415 
A oy ev As oi) A oe ne Pe ee een ene <n ee See ee TEMES SP TET SUREPOS he A Bog 47 
CCy is ee : reel ee are ee See ee aioe TTT ier a eed oh on Wer. 460 
gh 1 A a eee ere ke Lo ncn ene te MPM Le eS Te CAM ye dec et - 144 
RGF y Saat, ! J Lise pctdh cress shale lca cae ee, at ea leans cE Za cab aay Dk Gos aoe See ee 48, 144 
KMICOES, CD cites siysievscl Ss 0a Settee ee cheater ey She occas cpus Pree ce ke ade care 455 
SCTE Of © Son nes aera eee. Sa ae oe a See ane, Maremma enn i mM, RO As yp a a 456 
L 

BEB CEW, LRA J haeties, hrerainty pap aa ct peaatae ge ca iat ae gh es Ree ace Ae dk eA 72, 284, 285, 331 
jE tyol slog oe ol Sears ae eee ee Nae ae eee ene Ome SEOs WENN We eA EMR FEE oe eegay ey ac ee 3S 40 
BO CC Pe Fe olor ch aes ody arash nyo, axeetn ont Fk eesiceipay'S eueg aah oleae, aca olan a) ace in te 315 
Rrra eh Wi Racks 45 sissy Goss loco io Ay hs begat gee eed ga Sen a) ey ge 312 
DPA SONS IVE 5s Space Se, ns ck ay og Syecsearey aes were tabetha acto ee go relink ag eh ee ae oe te cece cr rae a 462 
Bat ax TRS NS a sash) ox ces sy nscsestes eA a cleat ahaa cy ty sol cred ee aR EL OR es RC ST arate 18 
Wautenschlager; RoAw coos 4 <Sags «wi ahatw Skane vada an ene eRe © nse ke She acl a ee 426 
A WSOUU AIRS 168 Soret .% ty a ceenc, silence) ee Scaueasien od est cutee 0 eae tcl acu erent ae 24, 31, 307 
ReB Aarons Ws eww a bee kaa Ssae Sed ec ee ey cn ee A ee eS Ae a ee ee ee 6 
POS Tear > IR egie cachivay esi ce sactero tere cae rho hapa oh ao Gee Sol aes a cc ad Rg oe rr 445 
ieee Robie UN. gars aes Aacotncs Sn aie uclay ok oe ected mu een ny AU gE les ee La cee 406 
Pete Tt U2 OS 5 Gy be hve Soars ave ck, slpalec, Shel SAA a pa cae ras in Raa A 297 
Ree pplaN, Cos sees icin sation do thon, Seale oie epay yeeeeintin ein Veh a ctaURare oth ep ate tyes ite ae eas Bt ee 144 
| 01 Be ee ee Ree ir ee Norse, hue Ce NEL Hert Mn Me Gem kn 45, 263 
(ewistd Bt i Wash CoN, gO 0 ie a5 sce ass can ea eS ee en 104, 424, 428, 450 
PIS UG ine i isch ot tls gle Bodega apeeae Peck Osc mae AR UATE arf OAL. cu ceca an eve le ean tg ean en 291 
Pe DH ONG SAM = sie 538 aid ax seiftee sens tues 3b eateh a eee ae eee ere he 421 
Lindegren, JBise fap cigs eo see achcerttel etl rnc cae eh areca Pc eke 68, 277-279, 294 
Waricligr eins Re a esses. wha. sea hs eh 2 clea Sas Ue eae YI CR oa cacao carts Ne eee 463 
Retro tds EIB sate ase y wh shore SoG dace, tad seeks ace ees i cee eat ge ee 2a 22 
Beane SPD) Rei sat vi sonia war asb ashen oer alot Gnade hg ie ee ao ee ce 272 
Wo feren,. CF 5:.. Weep sls, Sh weve pv ay hah, Se A a, aces pute eames) este ae eee ea ee 287 
ong eG EP Rs, DO AB ac thn Gotsserh cis, apa Roe n ea aneuaee eee Vaan negate ete ete aa ee 443 
| Bs) Ce kat, Coe eee rene Pere era Me Ra epee em aman Vea eee eR ne ant See Meyda oo acs 285 
Woutondes, Shia. s so iae ght teas ot geek ae a ie en eke ete ete ae 301, 302 
DROW PRS EE ic ca 'esikoysn, aidlbay ples selene cau atcurce es eibaag ean aba ar a ee Ro ne tee ee 284 
PATO Rie badge ska sc heap dec VSy sea nena MGA AR cetacean earnestness 144 
Baum ern RR Dy oa es s,s seit ute ecto esa tg ee Pe trea agree a 93 
tae © eo ne ce ae mens were Varghese ny OP me deere Be 313 
Tus ys, WR ios.scyh 2e aglow aul ote syaas Spare a sw hsipee ete oa ae nea et cana te caine 5 Ok Sei ae 303 
is ae OS 6 ee re ee earn oer me Mere enone ree ey We ree Cee ety nh eee le ye 88 
Mayan Di Bee \ ste dow spss ea tapeny ies: died ows iS a Ae ae eee oe ee en 301-305 


640 


M 


ZI TUS Ba ssa Tot SiR SU oes A PO ete Ges ie rr Ald 38, 79, 84, 85 
UN ORTAVONE, GENIE. pis Sug.cduttndcsey sll of fel Ot gy Co Rene ete nicl CIR ng nC a 144 
EIST) |e yo an hags 205g He di BAe ly pepe omits cy C7 eg AR er a 2 144 
Pea ONG 2 eee ee ee ee POs e Cae Ain pieces Ws etn av aie ih b ouvob 8 4-0 a Bred ae ee a HA ve 330 
Paes INA ee a a Ae eet an wal L's hts wsius bow OY AKO a sad Ca RS ORES 330 
Pea 58 Tan Or ree re PRR 1 ee De he ts ile ee Wik a wid Sw bo Ga ad ble oy Ae wis aden 40 
Ree eae ee Te Se ee PE eT AUER Alc) fie MOA Rs 0 4c Gh sw MB a ed ebm + Bem 8 
SUERTE VST NU TBLES 5 2 G0 iy as uh 29 A al a A SEI ee a a 437 
aR AR VV me ema eee ee res ae RES ihe ye Se siig us hs bce ack cbr aca's & wasn aa BERLE yd dor 300, 323 
ee a ey EE CPR ee ons or) Eire sce fo he) Fy 4, 4% m8 Sane 6 Gyn 4 HH pes 459-461 
PIGSSETERES Bboy ycls Since SiG ct cake ieee eo 462 
CAI TRE Mo AED 0 oe er ei ee lel ley ae ea 433-435, 445, 446, 449 
a ee ce ae toate Pe tra eee Bcd See Gih Gs p's ear k buds 4a hwo ae 100, 404-406 
Fo il he eee Nn ee PER eR ean Cok hati s is vags Hietirs ooh ew dates ge sop alee Meee 285 
aE cies NN ety fer Ate eine el Satis sh aK eRe oh ack Nh whch dd 4 ve we pagal 439 
ee a eR Bent ae baa a eee ex ROME G6 Coa aha eauie: hv eC Rfe\iissk BA ae 64 do eal Powrale wig, a > 324 
eR VTL BOE ues guldogagast tyes lie Bika Why ELE eek noha, Gesell Geta tie Saree ki uP ce 424 
CST YS oe, less Bi Gai ie ae ee Sr ner re ee ae re 302 
Ee Ce NR iat AN curr rat cue eR iret ee ee Foca ARMED ed cs Sis hme coe oom 4 en Bee Btye arc’ 287 
De ee CELE a VLG VV Ey eee ec Ong rn EPs Se ea OS hl & ass ions SL QUE o's due vce whe 420, 445 
ate ATT TLONM Ve A Mr reek ane ait nc Cayce doe ‘x my abs > ota ae RIBIE A 8 Oh swt ape Agta 292 
Perera ACE VA |) re eT Ne geet eden es Sisto dh gPiais ad so. nh We avin ods Geel 2.6 we yoy gs Veg, he 450 
RO eae ee, er eT CU Shon ns 5. Siiekg' wine ok @-dysile, Sl GALA dela ¢ edo FOR 308, 310 
ATTAINS Ca RIEE 51 natch BULA S Ge ab bie nin GCAO aR PNP nn Sc 14 
NES FY ot 4 IE Ble il Bc Berle aR Ao Oe ee ene), a a rs 411, 445 
WFO) US CT RR Ete Atel Ale 2 evde Bghee cc Sie On vee Ae imp ta cel en a 285, 295 
PLN NGI RL UGTA olay as ceraie 2 i gelhaieg Oo) OAS te lle UNNI i ea See a ee ee ee 425, 431 
AG RCC Ree (are RIN eae itr yh Lie Wena e, fou sachs ud ands. ¢ 4. aha du mw leva. «valle, Wan ahaha’ ou 81 
ae re eR Ss ial psa PAS athe o BIE aly vie RUM SOG pithy Ww Sled eR wee 459 
Ao Lees ee en er Me ten Sigs haan, hyo ange tie sik ars Bde th a = hw Fis Ss ols, aaa 134, 143 
Pe eEOEETOTIGOUY CV SMR TO ata fe eR ee tes te cinkGieee en ntone sfad-ale Gc A abo ably & 131, 142, 144 
Py ee ee ee ee aE em o's haus once vale re tush d ae © poem S b a-g abies dt mt nie « efu a poh EU 92 
ae eee GM oe a Pe ed SES es en onstle Tek Seles < © denice lege ia 4 tah Aw Gia 8 wd avel@hs 121, 142, 144 
WRPG TTS. UGS oS. samtc deste gl thee el Seat 4 So RUBS cae wena tne RnaE RE 2a CO meet ee 297 
el NGC No sme Ne et ce ee Ce errr cee Sb ae vce dys, isatlclia We bae «Bs trefane, an a ee oo he Gale a Gh ae 2 
PA eer NC 5 OD eT Serre, A EG ee he a ti EROS Aes 45h 4 Ra a + + ag hg, ep 454 
ska FEEL BEE. 1, ol a cele ate RA ROPE co vaegg ce, eet URRNMGS rs Pn ara einen gn ler naar rN 328 
Cera veteran IM Ns oy la eee Sle Sa tk A 8 A ON ict er alee ar eee ee ee 438 
“SECTS, AS. on nah, © Sibee Vaag ROMS AS a OR ness ne ee le ale eee nc ee 461 
SE ESS: UERMClSe 5 Bagy A ee a RS oe Sa A ie 2 i a eer Pa a 54 
erate a Le eR ae ee ree ed ate ace Sa eh acts ee ASG a SPaGh a Aid ols'w a wine's 4 Maly cM Syatiegs 280 
Wevnstere, GC oo ee hn Wahl aS De aA ot a oo Ea a oe ne ie ear ea er oe 406-409 
ree Se eee Vi IY a de er rene ely he te la nn OEE LS Aes Ay-ng od vos sd Se es 2 8 OE eee 8 
N 

Pea Sen ie NP te ern Me aie Rn ee stat Baye was diss 9 Xie enlace wh SO Ae 6 Owe we SOS we 286 
re ote 2 Ca a Ny MI re 8 Een ore a te ak oly Be ovegia neste were ara nn eS Se Eee Bs pes, ans 65 
a eee PSN ie cli oe BS ha a)sf eee Sa oho ok wig veh naw 8 opal 33, 66-68 
Racy Ata A en ta fie ye shalt eT Vat PE ke ain ane ee od Ge Od pd so dn 20, 296 
Satin Gk. Sy stn ns a We athe aoe Be Ne ree ae ie ane 452 
YUSPREL TEM: ac ale & gel ek Rocca leh Sa te cee ce ee cee 269 
SRDRIEN IE, oul Yee oo Sp Oc 5 ha) Surah Oe ames oer ROR MRE yc ae eet ea re a a 40 
O 

Mav si britale Ee lo auataesip he cr POLO HOO a Ace OCC na cn a ea 303 
OYONSI, PIM 2 do Se WBS a0 et Ione eee te 421, 422 


641 


ODES G. Boece cues be Pe hehe Bales Bec tots emia Bae oe ee de Ee eee en a 421 


©) Ta 0 Dene naar are Cer aria irr oe re tee rma Me erg leit tir circ Oe aero ed koa 89 
Oman, PLOW. as sched eae be ee Pe ek ee ere te Fre ek © chlo oe ie ake Ee cop are en aa eo 25 
Ouyer MT as ei dhs 6 Ao OOo ee wie ere Melee See Fa one lle Oe aNnneL enya RENTS CaN eRe earn ee 47 
P 

Papavizas, G.Cy idk ce colds 4s pores Sei oe ohn Soe eke Cake hee ie enn at ae ao 40, 41, 92 
Parker Br sx d Se bien 0B 5) kb OI enalgnk CMR ae he 1m ee HRD EME Gk deg ee Orne oe te 422 
Parker, DoE 35 363 ae ET Oe Re me ee Sk a SU ae pete ee ee nen 441 
Parker, PELs 2 cos bsasscrs Banas Wee een eee eet ee De See anne eer ne 8, 15, 17, 18, 24537 
Parker Ea Bee s ccie ee Sats eee Ge oe Bo EB, le ak She SE ent Se cadtte P AOE er oe a on 24 
| of da be Sr in etd ey ee een ee ek eed bea Sol LBS hay: occ ove 411 
Patterson, RS. 6 hair w cusce ach, Bene a age WP Re etn er lene te | ee aig ke eee Laie A tnitote eca te eee ee 287 
Pecora, Pio a ei b See ea ee aoe ak BIR ee ee aN Rak eciee W atete In eee ite gene facie te 85 
Pemberton RoW cd cctic © opes Uk ocd gs re timed cee itr See eens Coke Shee na eer tay eal arene ena 55, 78, 79, 85 
PesKINS. Bly sk ee ae ee eS ee BR EEN POU lode FIO SANE on AER en eae oe a 37-39, 54, 78, 80 
POLE 56 Vii coc ok 2s bese thas Ha Ree rs St HN ee 8 er eet cece ete ee ee 408 
Petersen, Vides ew ote hae oe ce He eee ee tO ets Sage ay AO cre ae Ue 67, 294, 295 
Phillips! BoP etek ook eke cucre eRe ae ee een ae centre eop oie sarki See nh Ok 11, 296 
Pickard, (0. Sace 25.7 2 5c 8 bs Su, ee ee Bee oie eh eee Wg Ge 407 
opts a 8 eee nee aR to, Sear 8 A An te A eer ae NTRS eT ee we ol 80 
Plowman RoD ecg) 5 Oa ata ah Wein ae Reine eieewre 2 Eee OM Seige a ea ee ee ais ee care 142 
Podewatte, I2D ic ways avs alas See tue Wen wle due Gey oe OWE Sat in We aaa nas eek ec 424 
PONGED: Fe toed ao eld ae ae A Te CET ie OP aay ene GE PE 462 
Poprawski, D352). cucSankn's petae oo ate eter ce i-ce aie Bile crane oe maS ohne 0 eee My cath 329-331 
5s Gi ed tare eae mane eed aan rea, MLN a Mila UAL e eh ee RY Some cn MS 233 
PHSOV. BP Lon cae. foe @ ante gies «ewe Oe «a ee oR EEE. Sede SA ae Ne Seo ee a EAN RR ee 98 
PHCEhek Be oro ercaio  c.tae, S380 BON Se er ae eee RN RD Get aC toe Pe te gen 24, 29, 56, 57, 308 
Q 

Quednail, Faw wi. <5 «maa eh a ite etre s hee ler. Gee neath teeta, MRI Ry, Smee cree i 440, 441 
Quimby, Pox gee. ose ees tie ee % mete etl ei acres Pete ten SACP ede ot a oircl ARE a 79, 81 
R 

RA05 ViPS iis Sve oie sin ces = bef Sale Were eee ae er ead ep IR Rone, nee ee ee en 417 
Rathburn, He 2°): acl farciy Sere ea toe er one ete ete tee ae he re ote fe tn tone en ee 302 
Rapps. M.S. 0o aoe Fon eg ace erm eleita ae ee neat eke Mam chris ta la'te Siete, airs a wien ee Ne tee, ree 422 
Rearaon, Ri Sa avsccta Gem went wat Se Cee eRe ane Rend oe 9, CoD LT Cen eae ee ee 419, 426, 428, 450 
REDOIS, Re eieans cals 2 Ae Rlhey cllera maenceNae nee CEN ic tne reba ry cee elias ena 91 
RECA Dy Re ivi! « tee Sac eh apis eds kA cee ee yas geee ae anal Re er a we ce Fe Beas.» 
REGS) Neer oe c's /ela: ate oth to ately. alates aah te (bi aflsta aytemele gah Wrote Wyte eens tien am i uel oP Aa kel, ee 19 
REO VES) Si goce c aiece awn eumlatele capa ake taints Ce alee att ea eee SE A FARR ce, tanec CI Pe Pa ce, 404 
Richard? RD Seo ise heel tee oa  Oee eRe ge eA e PURO Ake Pn Renny a oc 123 
Ridgeway, Rie oi! 2 tac outs iste te En ae, a eee nl toast hae Clee ele ee ace Pati «ae hone ee 263 
Riles a oe 5 so Reem as cele tea NG ck ee eg 2 eee cc ann ae Oe ene ra ee a 462 
Riley. Ve is Stach a ee Mig RA 5 Pate en ty ee OLR, ter en oe 6, 95 
Rogers, CoB. tics Mie tamales Otis filets mle cet Muck etangc Tatar” Scents int esl Gels nn cs nae 68 
Rollinson, WiDiog op hed Tea hee ele ete ee ed a te 424 
Roorivaniykcy ING 8 sata ait a's eco ae ve 9 eal ot ol phate Int Soe gh ntl Oe ts oR RL Ik Re en 417 
Romine CLs i 5s ile aoe ates eaegeatees Mote dec ah aad ra Net ae ees tae oo oe 212 
Reomingery Re isis sie ihe aa ieee te age Rates als ie aR 4 me On Oe 152 
Rosenthal SiS cs iis atten, eae tte nee aac aha anaee nea eee ere eo ie celeste er ee Tre 78, 79, 85 
Ryans R. Bec iia ssn cond 2 oo, Std tafe eer he oe es era a ne nn 442, 443 
S 

Sater se Ro owe Siciy Sack tue a sale tat oe ete ta POM Peete tis OS, | lem ge ee ca 23, 24, 49, 50, 150 
Savage, KBs te cies G55. aoa «0, v4 Boss walle 'a ed liaise leaky nadie oe eee tale, oe ee ee 284 


642 


ee a ee se id as ties Gh bone ob ok eh EEN bee Roe bea so eats 40, 91 


Puede INE Web oo als Sab abs lat 8 le an CCIE BRE SAA ea ann 88 
Sy Biull AN Ess Cala haan ak Celta So) 5 ae te abe De Re a ie eS A a 55, 420, 421 
cern CLO re ane EL Ute Un Ree Gn eo hee Skt deel eb A -avS ln eed -e qed w kw Wa ERAS a we EO 101, 409 
SAME NCU VS ese er one ars ln a Gh Sik ats Sod Sate sie b gus la bo sFe Ba Goad @ alae wb 88 Vere, a 445 
Pe TETNNG 20 emma ee eect Ame ire eM Te VE Ke Uk fin scien Gus echo dodsca ters sk OP ACR a bcd 0s ole up 401, 443 
ENaE ee TAR NVan) MES ee oe ne UE Ree WR terse, 8 Ss ee) Bob ond 6 oie wi. GH ob 8yd RRS Wa ayncacg. 2 68 
ee eat tt ea ey eeotet oe etme NT TS ceth aria ye eisc Gs a lun FG e th wotea add ide oe lag Whe, darn dps bee 143 
eee GON 2B pipet ih ahd pleat ie oye cash wo Sh ee a eg a a 437 
Nek eT a weedeat ae Mee IE, Uwe Se cco devi Soe Gece eG sb) ae ord Ck > wv w OD A EEE Co 144 
SETS Cola 6 SBR ao evades o iv Sw G onc <7 SE Ree ae ae en ee 269 
a ES a oes ne er eee 2 FS Gia cues Lh Go hie une s Rahs Wd Wa DUG ap ee Swale ae eegnld (Es 
PSAETEN ee IME. Gaede aes ae By IOR cl ene A opi ca Sed eg en ge eg 302, 304, 306 
SS Ke or ee eee eg Sele oak c Wal Slee Fea 6 oP hed ses Sen ween 426 
SUT ETTUG Ve  e T ir h  aL  LAat  en eie  a 51, 297, 328 
COS RT abt mere ee eee ars Cee ete eed ise asd save ales be SON 4b Had ee sees 407, 408 
Beer OG et Sara mene ree RN etc ee s aeaPeoe Sat eee Sede |. ache cs op ev ey Gi dW gedies pv bd és Scebahe ee ae 426 
eae eck aia ree eae ee Er, PE ee rete on suntan oa, £ Winig Wile dude Oath wp Gas Bob we awlehs 40 
STATES LPL DN 5 koi 5 of, ldo aa Ceye, PEPER Acs CER ta nsaEC eo ron kOe ne. 16, 24 
SPACEUN, USUI. Ss", 2 Be co ve te eee No 4s Sa oem ca ee 
SYENTATS LE o a pedpecd Ali 6 en SRS CRMs HR, AeA ara ee 462 
eae Sa tel I aoe ae ee ee Mee SMM ohh SOS ok vg. hala sia ake ais dina le Gea 8 beeen 329 
Se SITETULUE®, a shane oh tng. er Res Gree, Aaeivee oe ito ei A ago 84, 85 
SHSUBTFOGIR, URIDY. se Sa 0 GaSe eee adel cael QARCn OEE Cas cE a a On 413 
eins CC ee ONS 0 cae game PO ee ite Mode 30) y's. alle «ae, SMEAR i sn AS Gs Gre’ ¥ a a kW A ye 30 
SOAPS TRUE. 215 Seka ooh Lae gam ales a Cie ge too a 47, 48, 56, 70, 72, 144, 159 
SPEIRS, IES 0 9 adie aN ogee Gy Aa 1S ir hee ara a On 454 
see eer re Ue eR aE yee aie le ne oPe Gite ra. Sev ne Shas mea 6, Sib wis d 4p wip Sots she 6 Wes ee 'e. = wi peY AVS 12 
OUT eLetter eI ee ary pW Se Mate ase ag Pees als ba wens a Be SER RVING vate pe 
SS STEEGIS, V8 ah sens eee: aap ch yo ed RCE ACHENED reyes LPR PC ee ne gg 96 
Seat Ary nt Cs fy eT eee ee ere, ee Nt se AG dk lp ae tos nee Gre a) ua wins edits Ala a/eIa dw wn ly nw DE ae 301 
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